Low cost industrial production of coagulation factor IX bioencapsulated in lettuce cells for oral tolerance induction in hemophilia B

Biomaterials

Volumn 70, Issue , 2015, Pages 84-93

  Su, Jin ^a   Zhu, Liqing ^b,d   Sherman, Alexandra ^b   Wang, Xiaomei ^b   Lin, Shina ^a   Kamesh, Aditya ^a   Norikane, Joey H ^c   Streatfield, Stephen J ^c   Herzog, Roland W ^b   Daniell, Henry ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c Fraunhofer USA CMB   (United States)

^d THE FIRST AFFILIATED HOSPITAL OF WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

CGMP plant production; Chloroplast; Hemophilia; Lettuce; Molecular pharming; Oral tolerance

Indexed keywords

CELLS; COAGULATION; COLD STORAGE; COVALENT BONDS; CYTOLOGY; DRUG DOSAGE;

CGMP PLANT; CHLOROPLAST; HEMOPHILIA; LETTUCE; MOLECULAR PHARMING; ORAL TOLERANCES;

COSTS;

BLOOD CLOTTING FACTOR 9; CYCLIC GMP; IMMUNOGLOBULIN E; ANTIGEN; MICROCAPSULE;

ANAPHYLAXIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHLOROPLAST; CONTROLLED STUDY; CULTIVAR; DISULFIDE BOND; DRUG DOSE ESCALATION; DRY WEIGHT; EXPRESSION VECTOR; FEEDING; FREEZE DRYING; GROUPS BY AGE; HEMOPHILIA B; HYDROPONICS; IMMUNE SYSTEM; IMMUNOLOGICAL TOLERANCE; INDUSTRIAL PRODUCTION; INTESTINE; LETTUCE; MALE; MOUSE; NANOENCAPSULATION; NONHUMAN; ORAL TOLERANCE INDUCTION; PLANT CELL; PLANT GENE; PRIORITY JOURNAL; PSBA GENE; REGULATORY T LYMPHOCYTE; SHELF LIFE; TRANSGENE; ANIMAL; BIOMASS; COST; CYTOLOGY; ECONOMICS; GENE VECTOR; INDUSTRY; METABOLISM; MICROCAPSULE; ORAL DRUG ADMINISTRATION; PLANT LEAF; PROTEIN FOLDING; PROTEIN STABILITY; SMALL INTESTINE;

ADMINISTRATION, ORAL; ANIMALS; ANTIGENS; BIOMASS; CAPSULES; CHLOROPLASTS; COSTS AND COST ANALYSIS; FACTOR IX; FREEZE DRYING; GENETIC VECTORS; HEMOPHILIA B; IMMUNE TOLERANCE; IMMUNOGLOBULIN E; INDUSTRY; INTESTINE, SMALL; LETTUCE; MICE; PLANT LEAVES; PROTEIN FOLDING; PROTEIN STABILITY;

EID: 84940847809     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.08.004     Document Type: Article

References (45)

1. Walsh G. Biopharmaceutical benchmarks. Nat. Biotechnol. 2014, 32:992-1000.
2. Jin S.X., Daniell H. Engineered chloroplast genome just got smarter. Trends Plant Sci. 2015, 10.1016/j.tplants.2015.07.004.
3. Chan H.T., Daniell H. Plant-made vaccines against human diseases- are we there yet?. Plant Biotechnol. J. 2015, (in press).
4. Kwon K.C., Verma D., Singh N.D., Herzog R., Daniell H. Oral delivery of human biopharmaceuticals, autoantigens and vaccine antigens bioencapsulated in plant cells. Adv. Drug Deliv. Rev. 2013, 65:782-799.
5. Kwon K.C., Nityanandam R., New J.S., Daniell H. Oral delivery of bioencapsulated exendin-4 expressed in chloroplasts lowers blood glucose level in mice and stimulates insulin secretion in beta-TC6 cells. Plant Biotechnol. J. 2013, 11:77-86.
6. Arlen P.A., Falconer R., Cherukumilli S., Cole A., Cole A.M., Oishi K.K., et al. Field production and functional evaluation of chloroplast-derived interferon-α2b. Plant Biotechnol. J. 2007, 5:511-525.
7. Martens E.C., Lowe E.C., Chiang H., Pudlo N.A., Wu M., McNulty N.P., et al. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol. 2011, 9:e1001221.
8. Flint H.J., Bayer E.A., Rincon M.T., Lamed R., White B.A. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat. Rev. Microbiol. 2008, 6:121-131.
9. Limaye A., Koya V., Samsam M., Daniell H. Receptor-mediated oral delivery of a bioencapsulated green fluorescent protein expressed in transgenic chloroplasts into the mouse circulatory system. FASEB J. 2006, 20:959-961.
10. Ruhlman T., Ahangari R., Devine A., Samsam M., Daniell H. Expression of cholera toxin B-proinsulin fusion protein in lettuce and tobacco chloroplasts - oral administration protects against development of insulitis in non-obese diabetic mice. Plant Biotechnol. J. 2007, 5:495-510.
11. Verma D., Moghimi B., LoDuca P.A., Singh H.D., Hoffman B.E., Herzog R.W., et al. Oral delivery of bioencapsulated coagulation factor IX prevents inhibitor formation and fatal anaphylaxis in hemophilia B mice. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7101-7106.
12. Sherman A., Su J., Shina L., Wang X., Herzog R.W., Daniell H. Suppression of inhibitor formation against FVIII in a murine model of hemophilia A by oral delivery of antigens bioencapsulated in plant cells. Blood 2014, 124:1659-1668.
13. + T cells. Blood 2015, 125:2418-2427.
14. Shenoy V., Kwon K.C., Rathinasabapathy A., Lin S., Jin G., Song C., et al. Oral delivery of angiotensin-converting enzyme2 and angiotensin-(1-7) bioencapsulated in plant cells attenuates pulmonary hypertension. Hypertension 2014, 64:1248-1259.
15. Shil P.K., Kwon K.C., Zhu P., Verma A., Daniell H., Li Q. Oral delivery of ACE2/Ang-(1-7) bioencapsulated in plant cells protects against experimental uveitis and autoimmune uveoretinitis. Mol. Ther. 2014, 22:2069-2082.
16. Kohli N., Westerveld D.R., Ayache A.C., Verma A., Shil P., Prasad T., et al. Oral delivery of bioencapsulated proteins across blood-brain and blood-retinal barriers. Mol. Ther. 2014, 22:535-546.
17. Berntorp E., Shapiro A.D. Modern haemophilia care. Lancet 2012, 379:1447-1456.
18. DiMichele D.M. Immune tolerance in haemophilia: the long journey to the fork in the road. Br. J. Haematol. 2012, 159:123-134.
19. Scott D.W., Pratt K.P., Miao C.H. Progress toward inducing immunologic tolerance to factor VIII. Blood 2013, 121:4449-4456.
20. DiMichele D. Inhibitor development in haemophilia B: an orphan disease in need of attention. Br. J. Haematol. 2007, 138:305-315.
21. Dolgin E. Immunology: oral solutions. Nature 2014, 515:S166-S167.
22. Ruhlman T., Verma D., Samson N., Daniell H. The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol. 2010, 152:2088-2104.
23. Daniell H. Transgene containment by maternal inheritance: effective or elusive?. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:6879-6880.
24. Kumar S., Daniell H. Engineering the chloroplast genome for hyperexpression of human therapeutic proteins and vaccine antigens. Methods Mol. Biol. 2004, 267:365-383.
25. Verma D., Samson N.P., Koya V., Daniell H. A protocol for expression of foreign genes in chloroplasts. Nat. Protoc. 2008, 3:739-758.
26. Markusic D.M., Brad E., Hoffman B.E., Perrin G.Q., Nayak S., Wang X., et al. Effective gene therapy for haemophilic mice with pathogenic factor IX antibodies. EMBO Mol. Med. 2013, 5:1698-1709.
27. Wang X., Moghimi B., Zolotukhin I., Morel L.M., Cao O., Herzog R.W. Immune tolerance induction to factor IX through B cell gene transfer: TLR9 signaling delineates between tolerogenic and immunogenic B cells. Mol. Ther. 2014, 22:1139-1150.
28. Wirz H., Sauer-Budge A.F., Briggs J., Sharpe A., Sudong S., Sharon A. Automated production of plant-based vaccines and pharmaceuticals. J. Lab. Autom. 2012, 17:449-457.
29. Daniell H., Lee S.B., Panchal T., Wiebe P.O. Expression of the native cholera toxin B subunit gene and assembly as functional oligomers in transgenic tobacco chloroplasts. J. Mol. Biol. 2001, 311:1001-1009.
30. Tsuji T., Watanabe K., Miyama A. Monomer of the B subunit of heat-labile enterotoxin from enterotoxigenic Escherichia coli has little ability to bind to GM1 ganglioside compared to its coligenoid. Microbiol. Immunol. 1995, 39:817-819.
31. Kraehenbuhl J.P., Hopkins S.A., Kernéis S., Pringault E. Antigen sampling by epithelial tissues: implication for vaccine design. Behring Inst. Mitt. 1997, 98:24-32.
32. Rescigno M., Urbano M., Valzasina B., Francolini M., Rotta G., Bonasio R., et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2001, 2:361-367.
33. Dénes B., Fodor I., Langridge W.H.R. Persistent suppression of type 1 diabetes by a multicomponent vaccine containing a cholera toxin B subunit-autoantigen fusion protein and complete Freund's adjuvant. Clin. Dev. Immunol. 2013, 10.1155/2013/578786.
34. Arakawa T., Yu J., Chong D.K., Hough J., Engen P.C., Langridge W.H. A plant-based cholera toxin B subunit-insulin fusion protein protects against the development of autoimmune diabetes. Nat. Biotechnol. 1998, 16:934-938.
35. Stål P., Befrits R., Rönnblom A., Danielsson Å., Suhr O., Ståhlberg D., et al. Clinical trial: the safety and short-term efficacy of recombinant cholera toxin B subunit in the treatment of active Crohn's disease. Aliment. Pharmacol. Ther. 2010, 31:387-395.
36. Hill D.R., Ford L., Lalloo D.G. Oral cholera vaccines: use in clinical practice. Lancet Infect. Dis. 2006, 6:361-373.
37. Stanford M., Whittall T., Bergmeier L.A., Lindblad M., Lundin S., Shinnick T., et al. Oral tolerization with peptide 336-351 linked to cholera toxin B subunit in preventing relapses of uveitis in Behcet's disease. Clin. Exp. Immunol. 2004, 137:201-208.
38. Goto N., Maeyama J., Yasuda Y., Isaka M., Matano K., Kozuka S., et al. Safety evaluation of recombinant cholera toxin B subunit produced by Bacillus brevis as a mucosal adjuvant. Vaccine 2000, 18:2164-2171.
39. Mbongue J.C., Nicholas D.A., Zhang K., Kim N.-S., Hamilton B.N., Larios M., et al. Induction of indoleamine 2, 3-dioxygenase in human dendritic cells by a cholera toxin B subunit-proinsulin vaccine. PLoS One 2015, 10:e0118562.
40. + T cells. Nat. Med. 2006, 12:627-635.
41. Scurr M., Ladell K., Besneux M., Christian A., Hockey T., Smart K., et al. Highly prevalent colorectal cancer-infiltrating LAP {thorn} Foxp3 T cells exhibit more potent immunosuppressive activity than Foxp3 {thorn} regulatory T cells. Mucosal Immunol. 2014, 7:428-439.
42. Iamtham S., Day A. Removal of antibiotic resistance genes from transgenic tobacco plastids. Nat. Biotechnol. 2000, 18:1172-1176.
43. Day A., Goldschmidt-Clermont M. The chloroplast transformation toolbox: selectable markers and marker removal. Plant Biotechnol. J. 2011, 9:540-553.
44. Shao M., Kumar S., Thomson J.G. Precise excision of plastid DNA by large serine recombinase Bxb1. Plant Biotechnol. J. 2014, 12:322-329.
45. Larson P.J., Stanfield-Oakley S.A., VanDusen W.J., Kasper C.K., Smith K.J., Monroe D.M., et al. Structural integrity of the γ-carboxyglutamic acid domain of human blood coagulation factor IXa is required for its binding to cofactor VIIIa. J. Biol. Chem. 1996, 271:3869-3876.