Low cost delivery of proteins bioencapsulated in plant cells to human non-immune or immune modulatory cells

Biomaterials

Volumn 80, Issue , 2016, Pages 68-79

  Xiao, Yuhong ^a   Kwon, Kwang Chul ^a   Hoffman, Brad E ^b   Kamesh, Aditya ^a   Jones, Noah T ^b   Herzog, Roland W ^b   Daniell, Henry ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

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

Author keywords

Cell penetrating peptides; Chloroplasts; Molecular farming; Protein drug delivery

Indexed keywords

CELL CULTURE; COLD STORAGE; COSTS; CYTOLOGY; DIGESTIVE SYSTEM; PEPTIDES; PLANT CELL CULTURE; PROTEINS; PURIFICATION;

CELL-PENETRATING PEPTIDE; CHLOROPLASTS; EPITHELIAL CELLS; MOLECULAR FARMING; PATIENT COMPLIANCE; PROTEIN DRUG DELIVERY; PROTEIN PURIFICATION; RECEPTOR-BINDING PROTEINS;

CELLS;

BINDING PROTEIN; CELL PENETRATING PEPTIDE; DENDRITIC CELL PEPTIDE; GM1 RECEPTOR BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; PEPTIDE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CELL SURFACE RECEPTOR; GANGLIOSIDE RECEPTOR; HYBRID PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ENCAPSULATION; CHLOROPLAST; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC CELL; DRUG DELIVERY SYSTEM; FEMALE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; INTESTINE EPITHELIUM CELL; INTESTINE VILLUS; KIDNEY CELL; MOUSE; NONHUMAN; PANCREAS CELL; PLANT CELL; PRIORITY JOURNAL; PROTEIN TRANSPORT; ANIMAL; C57BL MOUSE; CELL LINE; CYTOLOGY; ECONOMICS; GENETICS; IMMUNE SYSTEM; METABOLISM; MOLECULAR MODEL;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; CELL-PENETRATING PEPTIDES; DRUG DELIVERY SYSTEMS; FEMALE; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNE SYSTEM; MICE, INBRED C57BL; MODELS, MOLECULAR; PLANT CELLS; RECEPTORS, CELL SURFACE; RECOMBINANT FUSION PROTEINS;

EID: 84951821818     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.11.051     Document Type: Article

References (68)

1. Walsh G. Biopharmaceutical benchmarks 2014. Nat. Biotechnol. 2014, 32:992-1000.
2. Jin S., Daniell H. Engineered chloroplast genome just got smarter. Trends Plant Sci. 2015, 20:622-640.
3. Chan H.T., Daniell H. Plant-made vaccines against human infectious diseases-Are we there yet?. Plant Biotechnol. J. 2015, 13:1056-1070.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. Sherman A., Su J., Lin S., 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.
10. + T cells. Blood 2015, 125:2418-2427.
11. Su J., Sherman A., Doerfler P.A., Byrne B.J., Herzog R.W., Daniell H. Oral delivery of acid alpha glucosidase epitopes expressed in plant chloroplasts suppresses antibody formation in treatment of Pompe mice. Plant Biotechnol. J. 2015, 13:1023-1032.
12. Boyhan D., Daniell H. Low-cost production of proinsulin in tobacco and lettuce chloroplasts for injectable or oral delivery of functional insulin and C-peptide. Plant Biotechnol. J. 2011, 9:585-598.
13. 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.
14. Shenoy V., Kwon K.C., Rathinasabapathy A., Lin S., Jin G., Song C., et al. Oral delivery of Angiotensin-converting enzyme 2 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. Zahid M., Robbins P.D. Protein transduction domains: applications for molecular medicine. Curr. Gene Ther. 2012, 12:374-380.
18. Khaja K., Robbins P. Comparison of functional protein transduction domains using the NEMO binding domain peptide. Pharmaceuticals 2010, 3:110-124.
19. Embury J., Klein D., Pileggi A., Ribeiro M., Jayaraman S., Molano R.D., et al. Proteins linked to a protein transduction domain efficiently transduce pancreatic islets. Diabetes 2001, 50:1706-1713.
20. Schwarze S.R., Ho A., Vocero-Akbani A., Dowdy S.F. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 1999, 285:1569-1572.
21. Mills C.D. M1 and M2 macrophages: oracles of health and disease. Crit. Rev. Immunol. 2012, 32:463-488.
22. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature 1998, 392:245-252.
23. Ingulli E., Mondino A., Khoruts A., Jenkins M.K. In vivo detection of dendritic cell antigen presentation to CD4+ T cells. J. Exp. Med. 1997, 185:2133-2141.
24. Luther S.A., Gulbranson-Judge A., Acha-Orbea H., Maclennan I.C.M. Viral superantigen drives extrafollicular and follicular B differentiation leading to virus-specific antibody production. J. Exp. Med. 1997, 185:551-562.
25. Kudo S., Matsuno K., Ezaki T., Ogawa M. A novel migration pathway for rat dendritic cells from the blood: hepatic sinusoids-lymph translocation. J. Exp. Med. 1997, 185:777-784.
26. Curiel T.J., Morris C., Brumlik M., Landry S.J., Finstad K., Nelson A., et al. Peptides identified through phage display direct immunogenic antigen to dendritic cells. J. Immunol. 2004, 172:7425-7431.
27. Banchereau J., Palucka A.K. Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 2005, 5:296-306.
28. Celluzzi C.M., Mayordomo J.I., Storkus W.J., Lotze M.T., Falo L.D. Peptide-pulsed dendritic cells induce antigen-specific CTL-mediated protective tumor immunity. J. Exp. Med. 1996, 183:283-287.
29. Kraehenbuhl J.P., Corbett M. Immunology. Keeping the gut microflora at bay. Science 2004, 303:1624-1625.
30. von Boehmer H. Oral tolerance: is it all retinoic acid?. J. Exp. Med. 2007, 204:1737-1739.
31. Weiner H.L. Oral tolerance: immune mechanisms and treatment of autoimmune diseases. Immunol. Today 1997, 18:335-343.
32. Annacker O., Coombes J.L., Malmstrom V., Uhlig H.H., Bourne T., Johansson-Lindbom B., et al. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J. Exp. Med. 2005, 202:1051-1061.
33. Biswas M., Sarkar D., Kumar S.R., Nayak S., Rogers G.L., Markusic D.M., et al. Synergy between rapamycin and FLT3 ligand enhances plasmacytoid dendritic cell-dependent induction of CD4+CD25+FoxP3+ Treg. Blood 2015, 125:2937-2947.
34. Kwon K.C., Verma D., Jin S., Singh N.D., Daniell H. Release of proteins from intact chloroplasts induced by reactive oxygen species during biotic and abiotic stress. PLoS One 2013, 8:e67106.
35. Verma D., Samson N.P., Koya V., Daniell H. A protocol for expression of foreign genes in chloroplasts. Nat. Protoc. 2008, 3:739-758.
36. Haider S.R., Sharp B.L., Reid H.J. A comparison of Tris-glycine and Tris-tricine buffers for the electrophoretic separation of major serum proteins. J. Sep. Sci. 2011, 34:2463-2467.
37. Lee S., Li B., Jin S., Daniell H. Expression and characterization of antimicrobial peptides Retrocyclin-101 and Protegrin-1 in chloroplasts to control viraland bacterial infections. Plant Biotechnol. J. 2011, 9:100-115.
38. Sanchez J., Holmgren J. Cholera toxin - a foe & a friend. Indian J. Med. Res. 2011, 133:153-163.
39. Magzoub M., Eriksson L.E., Gräslund A. Conformational states of the cell-penetrating peptide penetratin when interacting with phospholipid vesicles: effects of surface charge and peptide concentration. Biochim. Biophys. Acta 2002, 1563:53-63.
40. Roy A., Kucukural A., Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 2010, 5:725-738.
41. Noguchi H., Kaneto H., Weir G.C., Bonner-Weir S. PDX-1 protein containing its own antennapedia-like protein transduction domain can transduce pancreatic duct and islet cells. Diabetes 2003, 52:1732-1737.
42. Hessabi B., Ziegler P., Schmidt I., Hessabi C., Walther R. The nuclear localization signal (NLS) of PDX-1 is part of the homeodomain and represents a novel type of NLS. Eur. J. Biochem. 1999, 263:170-177.
43. Phillips G.N. Structure and dynamics of green fluorescent protein. Curr. Opin. Struct. Biol. 1997, 7:821-827.
44. Miyata T., Oshiro S., Harakuni T., Taira T., Matsuzaki G., Arakawa T., et al. Physicochemically stable cholera toxin B subunit pentamer created by peripheral molecular constraints imposed by de novo-introduced intersubunit disulfide crosslinks. Vaccine 2012, 30:4225-4232.
45. Lakshmi P.S., Verma D., Yang X., Lloyd B., Daniell H. Low cost tuberculosis vaccine antigens in capsules: expression in chloroplasts, bio-encapsulation, stability and functional evaluation in vitro. PLoS One 2013, 8:e54708.
46. Davoodi-Semiromi A., Schreiber M., Nalapalli S., Verma D., Singh N.D., Banks R.K., et al. Chloroplast-derived vaccine antigens confer dual immunity against cholera and malaria by oral or injectable delivery. Plant Biotechnol. J. 2010, 8:223-242.
47. William W.W. Biochemical and physical properties of green fluorescent protein. Green fluorescent Protein 2006, 39-65. Hoboken, New Jersey. second ed. M. Chalfie, S.R. Kain (Eds.).
48. 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.
49. Durzyńska J., Przysiecka Ł., Nawrot R., Barylski J., Nowicki G., Warowicka A., Musidlak O., Goździcka-Józefiak A. Viral and other cell-penetrating peptides as vectors of therapeutic agents in medicine. J. Pharmacol. Exp. Ther. 2015, 354:32-42.
50. Wernick N.L., Chinnapen D.J., Cho J.A., Lencer W.I. Cholera toxin: an intracellular journey into the cytosol by way of the endoplasmic reticulum. Toxins Basel 2010, 2:310-325.
51. Cho J.A., Chinnapen D.J., Aamar E., te Welscher Y.M., Lencer W.I., Massol R. Insights on the trafficking and retro-translocation of glycosphingolipid-binding bacterial toxins. Front. Cell Infect. Microbiol. 2012, 2:51.
52. Critchley D.R., Kellie S., Streuli C.H., Patel B., Ansell S., Pierce E., et al. The use of cholera toxin as a probe to study the organisation of ganglioside GM1 in membranes. Prog. Clin. Biol. Res. 1982, 102 pt A:397-407.
53. Wilson J.P. Surface area of the small intestine in man. Gut 1967, 8:618-621.
54. Holmgren J., Lönnroth I., Månsson J., Svennerholm L. Interaction of cholera toxin and membrane GM1 ganglioside of small intestine. Proc. Natl. Acad. Sci. U. S. A. 1975, 72:2520-2524.
55. Fishman P.H., Bradley R.M., Hom B.E., Moss J. Uptake and metabolism of exogenous gangliosides by cultured cells: effect of choleragen on the turnover of GM1. J. Lipid Res. 1983, 24:1002-1011.
56. Hadjiconstantinou M., Neff N.H. GM1 ganglioside: in vivo and in vitro trophic actions on central neurotransmitter systems. J. Neurochem. 1998, 70:1335-1345.
57. Yu R.K., Tsai Y.T., Ariga T. Functional roles of gangliosides in neurodevelopment: an overview of recent advances. Neurochem. Res. 2012, 37:1230-1244.
58. Yu J., Langridge W.H. A plant-based multicomponent vaccine protects mice from enteric diseases. Nat. Biotechnol. 2001, 19:548-552.
59. Noguchi H., Matsushita M., Matsumoto S., Lu Y.F., Matsui H., Bonner-Weir S., et al. Mechanism of PDX-1 protein transduction. Biochem. Biophys. Res. Commun. 2005, 332:68-74.
60. Noguchi H., Matsumoto S., Okitsu T., Iwanaga Y., Yonekawa Y., Nagata H., et al. PDX-1 protein is internalized by lipid raft-dependent macropinocytosis. Cell Transpl. 2005, 14:637-645.
61. Kaplan I.M., Wadia J.S., Dowdy S.F. Cationic TAT peptide transduction domain enters cells by macropinocytosis. J. Control Release 2005, 102:247-253.
62. Batchu R.B., Moreno A.M., Szmania S.M., Bennett G., Spagnoli G.C., Ponnazhagan S., et al. Protein transduction of dendritic cells for NY-ESO-1-based immunotherapy of myeloma. Cancer Res. 2005, 65:10041-10049.
63. Su Y., Zhang A.H., Li X., Owusu-Boaitey N., Skupsky J., Scott D.W. B cells "transduced" with TAT-fusion proteins can induce tolerance and protect mice from diabetes and EAE. Clin. Immunol. 2011, 140:260-267.
64. Calder P.C., Dimitriadis G., Newsholme P. Glucose metabolism in lymphoid and inflammatory cells and tissues. Curr. Opin. Clin. Nutr. Metab. Care 2007, 10:531-540.
65. 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.
66. Su J., Zhu L., Sherman A., Wang X., Lin S., Kamesh A., Norikane J.H., Streatfield S.J., Herzog R.W., Daniell H. Low cost industrial production of coagulation factor IX bioencapsulated in lettuce cells for oral tolerance induction in hemophilia B. Biomaterials 2015, 70:84-93.
67. Agrawal P., Verma D., Daniell H. Expression of Trichoderma reesei β-mannanase in tobacco chloroplasts and its utilization in lignocellulosic woody biomass hydrolysis. PLoS One 2011, 6:e29302.
68. Verma D., Jin S., Kanagaraj A., Singh N.D., Daniel J., Kolattukudy P.E., Miller M., Daniell H. Expression of fungal cutinase and swollenin in tobacco chloroplasts reveals novel enzyme functions and/or substrates. PLoS One 2013, 8:e57187.