Viral and murine interleukin-10 are correctly processed and retain their biological activity when produced in tobacco

BMC Biotechnology

Volumn 9, Issue , 2009, Pages

  Bortesi, Luisa ^a   Rossato, Marzia ^a   Schuster, Flora ^b   Raven, Nicole ^c   Stadlmann, Johannes ^d   Avesani, Linda ^a   Falorni, Alberto ^e   Bazzoni, Flavia ^a   Bock, Ralph ^f   Schillberg, Stefan ^c   Pezzotti, Mario ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b RWTH AACHEN UNIVERSITY   (Germany)

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

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

^e UNIVERSITY OF PERUGIA   (Italy)

^f MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORY; ANTI-INFLAMMATORY RESPONSE; ATTRACTIVE SYSTEMS; AUTOANTIGENS; AUTOIMMUNE DISEASE; BIOLOGICAL ACTIVITIES; CYTOKINE; CYTOKINES; DELIVERY SYSTEMS; ENDOPLASMIC RETICULUMS; IN-VITRO ASSAYS; INFLAMMATORY DISEASE; INTERLEUKIN-10; LEAF WEIGHTS; LOW COSTS; LOW MAINTENANCES; MACROPHAGE CELLS; MOUSE MODELS; MURINE PROTEINS; N-GLYCAN; ORAL ADMINISTRATIONS; PROTEIN PURIFICATIONS; RECOMBINANT PROTEINS; SCALE-UP; SIGNALING PATHWAYS; SUBCELLULAR TARGETING; THERAPEUTIC APPLICATIONS; THERAPEUTIC PROTEINS; TOBACCO PLANTS; TRANSGENIC; TRANSGENIC PLANTS; TRANSGENIC TOBACCO PLANTS; TRANSIENT EXPRESSIONS;

ANTIGENS; BIOACTIVITY; DIMERS; PURIFICATION; TOBACCO;

PROTEINS;

GLYCOPEPTIDASE; INTERLEUKIN 10; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIMERIZATION; ENDOPLASMIC RETICULUM; IMMUNOMODULATION; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT LEAF; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; TOBACCO; ANIMAL; BIOSYNTHESIS; CELL LINE; GENETIC TRANSFORMATION; GLYCOSYLATION; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN MULTIMERIZATION; TRANSGENIC PLANT;

MURINAE; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

ANIMALS; CELL LINE; GLYCOSYLATION; INTERLEUKIN-10; MICE; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; TOBACCO; TRANSFORMATION, GENETIC;

EID: 64549116714     PISSN: None     EISSN: 14726750     Source Type: Journal    
DOI: 10.1186/1472-6750-9-22     Document Type: Article

References (63)

1. Ma JK Barros E Bock R Christou P Dale PJ Dix PJ Fischer R Irwin J Mahoney R Pezzotti M Molecular farming for new drugs and vaccines. Current perspectives on the production of pharmaceuticals in transgenic plants EMBO Rep 2005, 6(7):593-599. 1369121 15995674 10.1038/ sj.embor.7400470
2. Arakawa T Chong DK Langridge WH Efficacy of a food plant-based oral cholera toxin B subunit vaccine Nat Biotechnol 1998, 16(3):292-297. 10.1038/nbt0398-292 9528012
3. Walmsley AM Arntzen CJ Plants for delivery of edible vaccines Curr Opin Biotechnol 2000, 11(2):126-129. 10.1016/S0958-1669(00)00070-7 10753769
4. Sprang S Bazan J Cytokine structural taxonomy and mechanisms of receptor engagement Curr Opin Struct Biol 1993, 3:815-827. 10.1016/ 0959-440X(93)90144-A
5. Fiorentino DF Zlotnik A Mosmann TR Howard M O'Garra A IL-10 inhibits cytokine production by activated macrophages J Immunol 1991, 147(11):3815-3822. 1940369
6. de Waal Malefyt R Haanen J Spits H Roncarolo MG te Velde A Figdor C Johnson K Kastelein R Yssel H de Vries JE Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression J Exp Med 1991, 174(4):915-924. 2118975 1655948 10.1084/jem.174.4.915
7. Asadullah K Sterry W Volk HD Interleukin-10 therapy - review of a new approach Pharmacol Rev 2003, 55(2):241-269. 10.1124/pr.55.2.4 12773629
8. Menassa R Kennette W Nguyen V Rymerson R Jevnikar A Brandle J Subcellular targeting of human interleukin-10 in plants J Biotechnol 2004, 108(2):179-183. 10.1016/j.jbiotec.2003.11.009 15129727
9. Menassa R Du C Yin ZQ Ma S Poussier P Brandle J Jevnikar AM Therapeutic effectiveness of orally administered transgenic low-alkaloid tobacco expressing human interleukin-10 in a mouse model of colitis Plant Biotechnol J 2007, 5(1):50-59. 10.1111/j.1467-7652.2006.00214.x 17207256
10. Wakkach A Cottrez F Groux H Can interleukin-10 be used as a true immunoregulatory cytokine? Eur Cytokine Netw 2000, 11(2):153-160. 10903794
11. Moore KW de Waal Malefyt R Coffman RL O'Garra A Interleukin-10 and the interleukin-10 receptor Annu Rev Immunol 2001, 19:683-765. 10.1146/ annurev.immunol.19.1.683 11244051
12. Lucas A McFadden G Secreted immunomodulatory viral proteins as novel biotherapeutics J Immunol 2004, 173(8):4765-4774. 15470015
13. Avesani L Falorni A Tornielli GB Marusic C Porceddu A Polverari A Faleri C Calcinaro F Pezzotti M Improved in planta expression of the human islet autoantigen glutamic acid decarboxylase (GAD65) Transgenic Res 2003, 12(2):203-212. 10.1023/A:1022947726557 12739888
14. Mitoma J Ito A The carboxy-terminal 10 amino acid residues of cytochrome b5 are necessary for its targeting to the endoplasmic reticulum Embo J 1992, 11(11):4197-4203. 556930 1396600
15. Schillberg S Zimmermann S Findlay K Fischer R Plasma membrane display of anti-viral single chain Fv fragments confers resistance to tobacco mosaic virus Molecular Breeding 2000, 6:317-326. 10.1023/A:1009697604758
16. Zhao J Onduka T Kinoshita JY Honsho M Kinoshita T Shimazaki K Ito A Dual subcellular distribution of cytochrome b5 in plant, cauliflower, cells J Biochem (Tokyo) 2003, 133(1):115-121.
17. Schouten A Roosien J van Engelen FA de Jong GA Borst-Vrenssen AW Zilverentant JF Bosch D Stiekema WJ Gommers FJ Schots A et al The C-terminal KDEL sequence increases the expression level of a single-chain antibody designed to be targeted to both the cytosol and the secretory pathway in transgenic tobacco Plant Mol Biol 1996, 30(4):781-793. 10.1007/BF00019011 8624409
18. Sack M Paetz A Kunert R Bomble M Hesse F Stiegler G Fischer R Katinger H Stoeger E Rademacher T Functional analysis of the broadly neutralizing human anti-HIV-1 antibody 2F5 produced in transgenic BY-2 suspension cultures FASEB J 2007, 21(8):1655-1664. 10.1096/fj.06-5863com 17327362
19. Zdanov A Schalk-Hihi C Gustchina A Tsang M Weatherbee J Wlodawer A Crystal structure of interleukin-10 reveals the functional dimer with an unexpected topological similarity to interferon gamma Structure 1995, 3(6):591-601. 10.1016/S0969-2126(01)00193-9 8590020
20. Moore KW Vieira P Fiorentino DF Trounstine ML Khan TA Mosmann TR Homology of cytokine synthesis inhibitory factor (IL-10) to the Epstein-Barr virus gene BCRFI Science 1990, 248(4960):1230-1234. 10.1126/ science.2161559 2161559
21. Mosmann TR Schumacher JH Fiorentino DF Leverah J Moore KW Bond MW Isolation of monoclonal antibodies specific for IL-4, IL-5, IL-6, and a new Th2-specific cytokine (IL-10), cytokine synthesis inhibitory factor, by using a solid phase radioimmunoadsorbent assay J Immunol 1990, 145(9):2938-2945. 2145365
22. Proglycan http://www.proglycan.com
23. SignalP 3.0 Server http://www.cbs.dtu.dk/services/SignalP/
24. Cassatella MA Gasperini S Bovolenta C Calzetti F Vollebregt M Scapini P Marchi M Suzuki R Suzuki A Yoshimura A Interleukin-10 (IL-10) selectively enhances CIS3/SOCS3 mRNA expression in human neutrophils: evidence for an IL-10-induced pathway that is independent of STAT protein activation Blood 1999, 94(8):2880-2889. 10515892
25. Ito S Ansari P Sakatsume M Dickensheets H Vazquez N Donnelly RP Larner AC Finbloom DS Interleukin-10 inhibits expression of both interferon alpha- and interferon gamma- induced genes by suppressing tyrosine phosphorylation of STAT1 Blood 1999, 93(5):1456-1463. 10029571
26. Berlato C Cassatella MA Kinjyo I Gatto L Yoshimura A Bazzoni F Involvement of suppressor of cytokine signaling-3 as a mediator of the inhibitory effects of IL-10 on lipopolysaccharide-induced macrophage activation J Immunol 2002, 168(12):6404-6411. 12055259
27. Vitale A Pedrazzini E Recombinant pharmaceuticals from plants: The plant endomembrane system as bioreactor Mol Interv 2005, 5(4):216-225. 10.1124/ mi.5.4.5 16123536
28. Barbante A Irons S Hawes C Frigerio L Vitale A Pedrazzini E Anchorage to the cytosolic face of the endoplasmic reticulum membrane: A new strategy to stabilize a cytosolic recombinant antigen in plants Plant Biotechnol J 2008, DOI: 10.1111/j.1467-7652.2008.00342.x 18444969
29. Petruccelli S Otegui MS Lareu F Tran Dinh O Fitchette AC Circosta A Rumbo M Bardor M Carcamo R Gomord V A et al 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 2006, 4(5):511-527. 17309727
30. Twyman RM Schillberg S Fischer R Transgenic plants in the biopharmaceutical market Expert Opin Emerg Drugs 2005, 10(1):185-218. 10.1517/14728214.10.1.185 15757412
31. Conrad U Fiedler U Compartment-specific accumulation of recombinant immunoglobulins in plant cells: An essential tool for antibody production and immunomodulation of physiological functions and pathogen activity Plant Mol Biol 1998, 38(1-2):101-109. 10.1023/A:1006029617949 9738962
32. Twyman RM Stoger E Schillberg S Christou P Fischer R Molecular farming in plants: Host systems and expression technology Trends Biotechnol 2003, 21(12):570-578. 10.1016/j.tibtech.2003.10.002 14624867
33. Menassa R Nguyen V Jevnikar A Brandle J A self-contained system for the field production of plant recombinant interleukin-10 Molecular Breeding 2001, 8:177-185. 10.1023/A:1013376407362
34. Patel J Zhu H Menassa R Gyenis L Richman A Brandle J Elastin-like polypeptide fusions enhance the accumulation of recombinant proteins in tobacco leaves Transgenic Res 2007, 16(2):239-249. 10.1007/ s11248-006-9026-2 17106768
35. Ma S Huang Y Yin Z Menassa R Brandle JE Jevnikar AM Induction of oral tolerance to prevent diabetes with transgenic plants requires glutamic acid decarboxylase (GAD) and IL-4 Proc Natl Acad Sci USA 2004, 101(15):5680-5685. 397475 15056761 10.1073/pnas.0307420101
36. Streatfield SJ Approaches to achieve high-level heterologous protein production in plants Plant Biotechnol J 2007, 5(1):2-15. 10.1111/ j.1467-7652.2006.00216.x 17207252
37. Moore KW O'Garra A De Waal Malefyt R Vieira P Mosmann TR Interleukin-10 Annu Rev Immunol 1993, 11:165-190. 10.1146/annurev.iy.11.040193.001121 8386517
38. Yoon SI Jones BC Logsdon NJ Walter MR Same structure, different function crystal structure of the Epstein-Barr virus IL-10 bound to the soluble IL-10R1 chain Structure 2005, 13(4):551-564. 10.1016/j.str.2005.01.016 15837194
39. Ding Y Qin L Kotenko SV Pestka S Bromberg JS A single amino acid determines the immunostimulatory activity of interleukin 10 J Exp Med 2000, 191(2):213-224. 2195749 10637267 10.1084/jem.191.2.213
40. Zdanov A Schalk-Hihi C Menon S Moore KW Wlodawer A Crystal structure of Epstein-Barr virus protein BCRF1, a homolog of cellular interleukin-10 J Mol Biol 1997, 268(2):460-467. 10.1006/jmbi.1997.0990 9159483
41. Bendtsen JD Nielsen H von Heijne G Brunak S Improved prediction of signal peptides: SignalP 3.0 J Mol Biol 2004, 340(4):783-795. 10.1016/ j.jmb.2004.05.028 15223320
42. Emanuelsson O Brunak S von Heijne G Nielsen H Locating proteins in the cell using TargetP, SignalP and related tools Nat Protoc 2007, 2(4):953-971. 10.1038/nprot.2007.131 17446895
43. Salek-Ardakani S Stuart AD Arrand JE Lyons S Arrand JR Mackett M High level expression and purification of the Epstein-Barr virus encoded cytokine viral interleukin 10: Efficient removal of endotoxin Cytokine 2002, 17(1):1-13. 10.1006/cyto.2001.0990 11886166
44. Hsu DH de Waal Malefyt R Fiorentino DF Dang MN Vieira P de Vries J Spits H Mosmann TR Moore KW Expression of interleukin-10 activity by Epstein-Barr virus protein BCRF1 Science 1990, 250(4982):830-832. 10.1126/science.2173142 2173142
45. Fitchette A Gomord V A C Faye L Distribution of xylosylation and fucosylation in the plant Golgi-apparatus Plant J 1994, 5(5):673-682. 10.1111/j.1365-313X.1994.00673.x
46. Pagny S Cabanes-Macheteau M Gillikin JW Leborgne-Castel N Lerouge P Boston RS Faye L Gomord V Protein recycling from the Golgi apparatus to the endoplasmic reticulum in plants and its minor contribution to calreticulin retention Plant Cell 2000, 12(5):739-756. 139924 10810147 10.1105/tpc.12.5.739
47. Lerouge P Cabanes-Macheteau M Rayon C Fischette-Laine AC Gomord V Faye L N-glycoprotein biosynthesis in plants: Recent developments and future trends Plant Mol Biol 1998, 38(1-2):31-48. 10.1023/A:1006012005654 9738959
48. Frigerio L Pastres A Prada A Vitale A Influence of KDEL on the fate of trimeric or assembly-defective phaseolin: Selective use of an alternative route to vacuoles Plant Cell 2001, 13(5):1109-1126. 135559 11340185 10.1105/tpc.13.5.1109
49. Sriraman R Bardor M Sack M Vaquero C Faye L Fischer R Finnern R Lerouge P 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 2004, 2(4):279-287. 10.1111/ j.1467-7652.2004.00078.x 17134389
50. Gomord V Denmat LA Fitchette-Laine AC Satiat-Jeunemaitre B Hawes C Faye L The C-terminal HDEL sequence is sufficient for retention of secretory proteins in the endoplasmic reticulum (ER) but promotes vacuolar targeting of proteins that escape the ER Plant J 1997, 11(2):313-325. 10.1046/j.1365-313X.1997.11020313.x 9076996
51. Triguero A Cabrera G Cremata JA Yuen CT Wheeler J Ramirez NI Plant-derived mouse IgG monoclonal antibody fused to KDEL endoplasmic reticulum-retention signal is N-glycosylated homogeneously throughout the plant with mostly high-mannose-type N-glycans Plant Biotechnol J 2005, 3(4):449-457. 10.1111/j.1467-7652.2005.00137.x 17173632
52. Floss DM Sack M Stadlmann J Rademacher T Scheller J Stoger E Fischer R Conrad U Biochemical and functional characterization of anti-HIV antibody-ELP fusion proteins from transgenic plants Plant Biotechnol J 2008, 6(4):379-391. 10.1111/j.1467-7652.2008.00326.x 18312505
53. Crofts AJ Leborgne-Castel N Hillmer S Robinson DG Phillipson B Carlsson LE Ashford DA Denecke J Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow Plant Cell 1999, 11(11):2233-2248. 144130 10559446 10.1105/tpc.11.11.2233
54. Riken BioResource Center - pBluescriptSKII+mIL-10 http://www2.brc.riken.jp/lab/dna/detail.cgi?rdbno=1476
55. Yang Z Chen M Wu R Fialkow LB Bromberg JS McDuffie M Naji A Nadler JL Suppression of autoimmune diabetes by viral IL-10 gene transfer J Immunol 2002, 168(12):6479-6485. 12055268
56. Koncz C Schell J The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector Mol Gen Genet 1986, 204:383-396. 10.1007/ BF00331014
57. Kapila J De Rycke R Van Montagu M Angenon G An Agrobacterium-mediated transient gene expression system for intact leaves Plant Science 1997, 122(1):101-108. 10.1016/S0168-9452(96)04541-4
58. Zambrinski P Joos H Gentello J Leemans J Van Montagu M Schell J Ti-plasmid vector for introduction of DNA into plant cells without altering their normal regeneration capacity Embo J 1983, 2:2111-2123.
59. Kolarich D Altmann F 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 2000, 285(1):64-75. 10.1006/ abio.2000.4737 10998264
60. Kolarich D Altmann F Sunderasan E Structural analysis of the glycoprotein allergen Hev b 4 from natural rubber latex by mass spectrometry Biochim Biophys Acta 2006, 1760(4):715-720. 16403599
61. Van Droogenbroeck B Cao J Stadlmann J Altmann F Colanesi S Hillmer S Robinson DG Van Lerberge E Terryn N Van Montagu M et al Aberrant localization and underglycosylation of highly accumulating single-chain Fv-Fc antibodies in transgenic Arabidopsis seeds Proc Natl Acad Sci USA 2007, 104(4):1430-1435. 1783127 17227846 10.1073/pnas.0609997104
62. PeptideMass http://www.expasy.org/tools/peptide-mass.html
63. Crepaldi L Gasperini S Lapinet JA Calzetti F Pinardi C Liu Y Zurawski S de Waal Malefyt R Moore KW Cassatella MA Up-regulation of IL-10R1 expression is required to render human neutrophils fully responsive to IL-10 J Immunol 2001, 167(4):2312-2322. 11490020