Spray-dried chitosan microparticles for cellular delivery of an antigenic protein: Physico-chemical properties and cellular uptake by dendritic cells and macrophages

Pharmaceutical Research

Volumn 30, Issue 6, 2013, Pages 1677-1697

  Kusonwiriyawong, Chirasak ^a,c   Lipipun, Vimolmas ^a   Vardhanabhuti, Nontima ^a   Zhang, Qiang ^b   Ritthidej, Garnpimol C ^a  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c RANGSIT UNIVERSITY   (Thailand)

Author keywords

cellular uptake; chitosan microparticles; dendritic cell; macrophage; spray dry

Indexed keywords

ANTIGEN; BOVINE SERUM ALBUMIN; CHITOSAN; NANOPARTICLE; POLY(ALPHA BUTYL CYANOACRYLATE); POLYGLACTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CELL TRANSPORT; CELL VIABILITY; CHEMICAL COMPOSITION; CHEMICAL PARAMETERS; CHEMICAL STRUCTURE; CONTROLLED STUDY; DENDRITIC CELL; DRUG DELIVERY SYSTEM; DRUG DOSAGE FORM COMPARISON; ENCAPSULATION; ENTRAPMENT EFFICIENCY; IMMUNE RESPONSE; IN VITRO STUDY; LC 50; MACROPHAGE; MOUSE; NONHUMAN; PARTICLE SIZE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN CONTENT; PROTEIN SECRETION; SPRAY DRYING; SURFACE CHARGE; SURFACE PROPERTY; TARGET CELL; ZETA POTENTIAL;

ANIMALS; ANTIGENS; CELL SURVIVAL; CELLS, CULTURED; CHITOSAN; DENDRITIC CELLS; DRUG DELIVERY SYSTEMS; HYDROGEN-ION CONCENTRATION; LACTIC ACID; MACROPHAGES; MICE; MICROSPHERES; NANOPARTICLES; PARTICLE SIZE; POLYGLYCOLIC ACID; POLYMERS; PROTEINS; SERUM ALBUMIN, BOVINE;

EID: 84877730337     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-013-1014-7     Document Type: Article

References (65)

1. Kumari A, Yadav SK, Yadav SC. Biodegradable polymeric nanoparticles based drug delivery systems. Colloid Surf B - Biointerfaces. 2010;75:1-18.
2. Tan ML, Choong PFM, Dass CR. Recent developments in liposomes, microparticles, and nanoparticles for protein and peptide drug delivery. Peptides. 2010;31:184-93.
3. Ataman-Önal Y, Munier S, Ganée A, Terrat C, Durand PY, Battail N, et al. Surfactant-free anionic PLA nanoparticles coated with HIV-1 p24 protein induced enhanced cellular and humoral immune responses in various animal models. J Control Release. 2006;112(2):175-85.
4. Cui CJ, Stevens VC, Schwendeman SP. Injectable polymer microspheres enhance immunogenicity of a contraceptive peptide vaccine. Vaccine. 2007;25(3):500-9.
5. Feng L, Qi MR, Zhou XJ, Maitani Y, Wang SC, Jiang Y, et al. Pharmaceutical and immunological evaluation of a single-dose hepatitis B vaccine using PLGA microspheres. J Control Release. 2006;112(1):35-42.
6. Jaganathan KS, Vyas SP. Strong systemic and mucosal immune response to surface-modified PLGA microspheres containing recombinant hepatitis B antigen administered intranasally. Vaccine. 2006;24(19):4201-11.
7. Rajkannan R, Arul V, Padma Malar EJ, Jayakumar R. Preparation, physicochemical characterization, and oral immunogenicity of Aβ (1-12), Aβ (29-40), and Aβ (1-42) loaded PLG microparticles formulations. J Pharm Sci. 2009;98(6):2027-39.
8. Damgé C, Maincent P, Ubrich N. Oral delivery of insulin associated to polymeric nanoparticles in diabetic rats. J Control Release. 2007;117(2):163-70.
9. Estevan M, Gamazo C, Martinez-Galen F, Irache JM. Stability of poly(ε-caprolactone) microparticles containing Brucella ovis antigens as a vaccine delivery system against brucellosis. AAPS PharmSciTech. 2008;9(4):1063-9.
10. Sonaje K, Italia JL, Sharma G, Bhardwaj V, Tikoo K, Ravi Kumar MNV. Development of biodegradable nanoparticles for oral delivery of ellagic acid and evaluation of their antioxidant efficacy against cyclosporine A-induced nephrotoxicity in rats. Pharm Res. 2007;24(5):899-908.
11. Arias JL, Gallardo V, Ruiz MA, Delgado AV. Ftorafur loading and controlled release from poly(ethyl-2-cyanoacrylate) and poly(butylcyanoacrylate) nanospheres. Int J Pharm. 2007;337(1-2):282-90.
12. Miyazaki S, Takahashi A, Kubo W, Bachynsky J, Löbenberg R. Poly n-butylcyanoacrylate (PNBCA) nanocapsules as a carrier for NSAIDs: in vitro release and in vivo skin penetration. J Pharm Pharmaceut Sci. 2003;6(2):240-5.
13. Ren F, Chen R, Wang Y, Sun Y, Jiand Y, Li G. Paclitaxel-loaded poly(n-butylcyanoacrylate) nanoparticle delivery system to overcome multidrug resistance in ovarian cancer. Pharm Res. 2011;28(4):897-907.
14. de Koker S, Lambrecht BN, Willart MA, van Kooyk Y, Grooten J, Vervaet C, et al. Designing polymeric particles for antigen delivery. Chem Soc Rev. 2011;40:320-39.
15. Cegnar M, Kos J, Kristl J. Cystatin incorporated in poly(lactide-co- glycolide) nanoparticles: development and fundamental studies on preservation of its activity. Eur J Pharm Sci. 2004;22(5):357-64.
16. Sturesson C, Carlfors J. Incorporation of protein in PLG-microspheres with retention of bioactivity. J Control Release. 2000;67(2-3):171-8.
17. van de Weert M, Hoechstetter J, Hennink WE, Crommelin DJA. The effect of a water/organic solvent interface on the structural stability of lysozyme. J Control Release. 2000;68:351-9.
18. Wei G, Lu LF, Lu WY. Stabilization of recombinant human growth hormone against emulsification-induced aggregation by Pluronic surfactants during microencapsulation. Int J Pharm. 2007;338:125-32.
19. Mi FL, Tan YC, Liang HF, Sung HW. In vivo biocompatibility and degradability of a novel injectable-chitosan-based implant. Biomaterials. 2002;23:181-91.
20. Kusonwiriyawong C, Pichayakorn W, Lipipun V, Ritthidej GC. Retained integrity of protein encapsulated in spray-dried chitosan microparticles. J Microencapsul. 2009;26(2):111-21.
21. O'Hagan DT, Singh M, Ulmer JB. Microparticle-based technologies for vaccines. Methods. 2006;40:10-9.
22. Xiang SD, Scholzen A, Minigo G, David C, Apostolopoulos V, Mottram PL, et al. Pathogen recognition and development of particulate vaccines: does size matter? Methods. 2006;40:1-9.
23. Bramwell VW, Perrie Y. Particulate delivery systems for vaccines: what can we expect? J Pharm Pharmacol. 2006;58:717-28.
24. Rice-Ficht AC, Arenas-Gamboa AM, Kahl-McDonagh MM, Ficht TA. Polymeric particles in vaccine delivery. Curr Opin Microbiol. 2010;13:106-12.
25. Zimmerman I. Possibilities and limitations of laser light scattering techniques for particle size analysis. In: Müller RH, Mehnert W, editors. Particle and surface characterization methods. Stuttgart: Medpharm; 1997. p. 19-26.
26. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72(1-2):248-54.
27. Amidi M, Mastrobattista E, Jiskoot W, Hennink WE. Chitosan-based delivery systems for protein therapeutics and antigens. Adv Drug Deliv Rev. 2010;62:59-82.
28. Barbour EK, Abdelnour A, Jirjis F, Faroon O, Farran MT. Evaluation of 12 stabilizers in a developed attenuated Salmonella Enteritidis vaccine. Vaccine. 2002;20(17-18):2249-53.
29. Kissmann J, Ausar SF, Rudolph A, Braun C, Cape SP, Sievers RE, et al. Stabilization of measles virus for vaccine formulation. Hum Vaccines. 2008;4(5):350-9.
30. Ohtake S, Martin RA, Saxena A, Lechuga-Ballesteros D, Santiago AE, Barry EM, et al. Formulation and stabilization of Francisella tularensis live vaccine strain. J Pharm Sci. 2011;100(8):3076-87.
31. Sarkar J, Sreenivasa BP, Singh RP, Dhar P, Bandyopadhyay SK. Comparative efficacy of various chemical stabilizers on the thermostability of a live-attenuated peste des petits ruminants (PPR) vaccine. Vaccine. 2003;21(32):4728-35.
32. Srirangsan P, Kawai K, Hamada-Sato N, Watanabe M, Suzuki T. Stabilizing effects of sucrose-polymer formulations on the activities of freeze-dried enzyme mixtures of alkaline phosphatase, nucleoside phosphorylase and xanthine oxidase. Food Chem. 2011;125:1188-93.
33. Thyagarajapuram N, Olsen D, Middaugh CR. Stabilization of proteins by recombinant human gelatins. J Pharm Sci. 2007;96(12):3304-15.
34. Thyagarajapuram N, Olsen D, Middaugh CR. The structure, stability and complex behavior of recombinant human gelatins. J Pharm Sci. 2007;96(12):3363-78.
35. Ameri M, Maa YF. Spray drying of biopharmaceuticals: stability and process considerations. Drying Technol. 2006;24:763-8.
36. Elversson J, Millqvist-Fureby A. In situ coating - an approach for particle modification and encapsulation of proteins during spray-drying. Int J Pharm. 2006;323:52-63.
37. Westerink MAJ, Smithson SL, Srivastava N, Blonder J, Coeshott C, Rosenthal GJ. ProJuvant™ (Pluronic F 127®/chitosan) enhances the immune response to intranasally administered tetanus toxoid. Vaccine. 2002;20:711-23.
38. Kang ML, Jiang HL, Kang SG, Guo DD, Lee DY, Cho CS, et al. Pluronic® F 127 enhances the effect as an adjuvant of chitosan microspheres in the intranasal delivery of Bordetella bronchiseptica antigens containing dermonecrotoxin. Vaccine. 2007;25:4602-10.
39. Collett JH, Weller PJ. Poloxamer. In: Wade A, Weller PJ, editors. Handbook of pharmaceutical excipients. Washington: American Pharmaceutical Association; 1994. p. 352-4.
40. Kusonwiriyawong C, van de Wetering P, Hubbell JA, Merkle HP, Walter E. Evaluation of pH-dependent membrane-disruptive properties of poly(acrylic acid) derived polymers. Eur J Pharm Biopharm. 2003;56:237-46.
41. Kohane DS, Anderson DG, Yu C, Langer R. pH-triggered release of macromolecules from spray-dried polymethacrylate microparticles. Pharm Res. 2003;20(10):1533-8.
42. Haining WN, Anderson DG, Little SR, von Bergwelt-Baildon MS, Cardoso AA, Alves P, et al. pH-triggered microparticles for peptide vaccination. J Immunol. 2004;173:2578-85.
43. Shu XZ, Zhu KJ. Chitosan/gelatin microspheres prepared by modified emulsification and ionotropic gelation. J Microencapsul. 2001;18(2):237-45.
44. Ko JA, Park HJ, Hwang SJ, Park JB, Lee JS. Preparation and characterization of chitosan microparticles intended for controlled drug delivery. Int J Pharm. 2002;249:165-74.
45. Gan Q, Wang T. Chitosan nanoparticle as protein delivery carrier - systematic examination of fabrication conditions for efficient loading and release. Colloid Surf B - Biointerfaces. 2007;59:24-34.
46. Malamud D, Drysdale JW. Isoelectric points of proteins: a table. Anal Biochem. 1978;86:620-47.
47. Righetti PG, Caravaggio T. Isoelectric points and molecular weights of proteins: a table. J Chromatog A. 1976;127:1-28.
48. Shu XZ, Zhu KJ. Controlled drug release properties of ionically cross-linked chitosan beads: the influence of anion structure. Int J Pharm. 2002;233:217-25.
49. Kelly SM, Price NC. The application of circular dichroism to studies of protein folding and unfolding. Biochim Biophys Acta. 1997;1338:161-85.
50. Sreerama N, Woody RW. Circular dichroism of peptides and proteins. In: Berova N, Nakanishi K, Woody RW, editors. Circular dichroism: principles and applications. New York: Wiley-VCH; 2000. p. 601-20.
51. Pelton JT, McLean LR. Spectroscopic methods for analysis of protein secondary structure. Anal Biochem. 2000;277:167-76.
52. Vauthier C, Dubernet C, Fattal E, Pinto-Alphandary H, Couvreur P. Poly(alkylcyanoacrylates) as biodegradable materials for biomedical applications. Adv Drug Deliv Rev. 2003;55:519-48.
53. Vauthier C, Labarre D, Ponchel G. Design aspects of poly(alkylcyanoacrylate) nanoparticles for drug delivery. J Drug Target. 2007;15(10):641-63.
54. Behan N, Birkinshaw C, Clarke N. Poly n-butyl cyanoacrylate nanoparticles: a mechanistic study of polymerizaiton and particle formation. Biomaterials. 2001;22:1335-44.
55. Chauvierre C, Labarre D, Couvreur P, Vauthier C. Plug-in spectrometry with optical fibers as a novel analytical tool for nanoparticles technology: application to the investigation of the emulsion polymerization of the alkylcyanoacrylate. J Nanopart Res. 2003;5:365-71.
56. Behan N, Birkinshaw C. Preparation of poly(butyl cyanoacrylate) nanoparticles by aqueous dispersion polymerization in the presence of insulin. Macromol Rapid Commun. 2001;22:41-3.
57. Graf A, McDowell A, Rades T. Poly(alkylcyanoacrylate) nanoparticles for enhanced delivery of therapeutics - is there real potential? Expert Opin Drug Deliv. 2009;6(4):371-87.
58. Illum L. Chitosan and its use as a pharmaceutical excipient. Pharm Res. 1998;15(9):1326-31.
59. Huang M, Khor E, Lim LY. Uptake and cytotoxicity of chitosan molecules and nanoparticles: effects of molecular weight and degree of deacetylation. Pharm Res. 2004;21(2):344-53.
60. Sovadinova I, Palermo EF, Huang R, Thoma LM, Kuroda K. Mechanism of polymer-induced hemolysis: nanosized pore formation and osmotic lysis. Biomacromolecules. 2011;12(1):260-8.
61. Reddy ST, Swartz MA, Hubbell JA. Targeting dendritic cells with biomaterials: developing the next generation of vaccines. Trends Immunol. 2006;27(12):573-9.
62. Alexis F, Pridgen E, Molnar LK, Farokhzad OC. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol Pharm. 2008;5(4):505-15.
63. Champion JA, Walker A, Mitragotri S. Role of particle size in phagocytosis of polymeric microspheres. Pharm Res. 2008;25(8):1815-21.
64. Thiele L, Merkle HP, Walter E. Phagocytosis and phagosomal fate of surface-modified microparticles in dendritic cells and macrophages. Pharm Res. 2003;20(2):221-8.
65. He C, Hu Y, Yin L, Tang C, Yin C. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials. 2010;31:3657-66.