Protein delivery: From conventional drug delivery carriers to polymeric nanoreactors

Expert Opinion on Drug Delivery

Volumn 7, Issue 1, 2010, Pages 63-78

  Balasubramanian, V ^a   Onaca, Ozana ^a   Enea, Ramona ^a   Hughes, David W ^a   Palivan, Cornelia G ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Liposomes; Nanoreactors; Polymeric carriers; Protein delivery

Indexed keywords

LIPOSOME; MICROSPHERE; NANOCARRIER; NANOPARTICLE; POLYMER;

DRUG DELIVERY SYSTEM; MICELLE; REVIEW; SCANNING ELECTRON MICROSCOPY;

DRUG CARRIERS; LIPOSOMES; MICROSCOPY, ELECTRON, SCANNING; NANOSTRUCTURES; POLYMERS; PROTEINS;

EID: 73649120651     PISSN: 17425247     EISSN: None     Source Type: Journal    
DOI: 10.1517/17425240903394520     Document Type: Review

References (125)

1. Cryan SA. Carrier-based strategies for targeting protein and peptide drugs to the lungs. J AAPS 2005;7(1):E20-41
2. Brasnjevic I, Steinbusch HWM, Schmitz C, Martinez MP. Delivery of peptide and protein drugs over the blood-brain barrier. Prog Neurobiol 2009;87:212-251
3. Rieux A, Fievez V, Garinot M, et al. Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach. J Control Release 2006;116:1-27
4. Shi Y, Li L. Current advances in sustained-release systems for parenteral drug delivery. Expert Opin Drug Deliv 2005;2:1039-1058
5. Langer R, Tirrell DA. Designing materials for biology and medicine. Nature 2004;428:487-492
6. Branco MC, Schneider JP. Self-assembling materials for therapeutic delivery. Acta Biomater 2009;5:817-831
7. Blanazs A, Armes SP, Ryan AJ. Self-assembled block copolymer aggregates: from micelles to vesicles and their biological applications. Macromol Rapid Commun 2009;30:267-277
8. Torchilin V. Multifunctional and stimuli-sensitive pharmaceutical nanocarriers. Eur J Pharm Biopharm 2009;71:431-444
9. Walde P, Ichikawa S. Enzymes inside lipid vesicles: preparation, reactivity and Applications. Biomed Eng 2001;18:143-177
10. Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nature Rev Drug Discov 2005;4(2):145-160
11. Immordino ML, Dosio F, Cattel L. Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential. Int J Nanomed 2006;1(3):297-315
12. Strother R, Matei D. Pegylated liposomal doxorubicin in ovarian cancer. Ther Clin Risk Manag 2009;5:639-650
13. Li M, Hanford MJ, Kim JW, Peeples TL. Amyloglucosidase enzymatic reactivity inside lipid vesicles. J Biol Eng 2007;1:4-9
14. Yoshimoto M, Sakamoto H, Yoshimoto N, et al. Stabilization of quaternary structure and activity of bovine liver catalase through encapsulation in liposomes. Enzyme Microb Technol 2007;41:849-858
15. Yoshimoto M, Sato M, Yoshimoto N, Nakao K. Liposomal Encapsulation of yeast alcohol dehydrogenase with cofactor for stabilization of the enzyme structure and activity. Biotechnol Progr 2008;24:576-582
16. Kamidate T, Komatsu K, Tani H, Ishida A. Estimation of the membrane permeability of liposomes via use of eosin Y chemiluminescence catalysed by peroxidase encapsulated in liposomes. Luminescence 2007;22:236-240
17. Yoshimoto M, Sakamoto H, Shirakami H. Covalent conjugation of tetrameric bovine liver catalase to liposome membranes for stabilization of the enzyme tertiary and quaternary structures. Colloids Surf B 2009;69:281-287
18. Wichmann C, Naumann PT, Spangenberg O, et al. Liposomes for microcompartmentation of enzymes and their influence on catalytic activity. Biochem Biophys Res Commun 2003;310:1104-1110
19. Badiee A, Jaafari MR, Samiei A, et al. Coencapsulation of CpG oligodeoxynucleotides with recombinant leishmania major Stress-Inducible Protein 1 in liposome enhances immune response and protection against Leishmaniasis in immunized BALB/c mice. Clin Vaccine Immunol 2008;15(4):668-674
20. Colletier JP, Chaize B, Winterhalter M, Fournier D. Protein encapsulation in liposomes: efficiency depends on interactions between protein and phospholipid bilayer. BMC Biotechnol 2002;2:9-14
21. Yoshimoto M, Wang S, Fukunaga K, Walde P. Preparation and characterization of reactive and stable glucose oxidase-containing liposomes modulated with detergent. Biotechnol Bioeng 2003;81(6):695-704
22. Graff A, Winterhalter M, Meier W. Nanoreactors from polymer stabilized liposomes. Langmuir 2001;17:919-923
23. Barenholz Y. Liposome application: problems and prospects. Curr Opin Colloid Interface Sci 2001;6:66-77
24. Kuroki Y, Shiratori M, Ogasawara Y, et al. Interaction of phospholipid liposomes with plasma membrane isolated from alveolar type II cells: effect of pulmonary surfactant protein A. Biochimica et Biophysica Acta 1996;1281:53-59
25. Werle M, Takeuchi H. Chitosan- aprotinin coated liposomes for oral peptide delivery: Development, characterisation and in vivo evaluation. Int J Pharm 2009;370:26-32
26. Dai C, Wang B, Zhao H, Li B. Preparation and characterization of liposomes-in-alginate (LIA) for protein delivery system. Colloids Surf B 2006;47:205-210
27. Cruz MEM, Gaspar MM, Martins MBF, Corvo ML. Liposomal superoxide dismutases and their use in the treatment of experimental arthritis. Methods Enzymol 2005;391:395-413
28. Takeuchi H, Matsui Y, Sugihara H, et al. Effectiveness of submicron-sized, chitosan-coated liposomes in oral administration of peptide drugs. Int J Pharm 2005;303:160-170
29. Rengel RG, Grcic JF, Cepelak I, et al. The effect of liposomes with superoxide dismutase on A2182 cells. Eur J Pharm Biopharm 2005;60:47-51
30. Zhang J, Wang S. Topical use of Coenzyme Q10 loaded liposomes coated with trimethyl chitosan: Tolerance, precorneal retention and anti-cataract effect. Int J Pharm 2009;372:66-75
31. Jubeh TT, Antler S, Haupt S, et al. Local prevention of oxidative stress in the intestinal epithelium of the rat by adhesive liposomes of superoxide dismutase and tempamine. Mol Pharmacol 2005;2(1):2-11
32. Stadler B, Chandrawati R, Price AD, et al. A Microreactor with thousands of subcompartments: Enzyme-loaded liposomes within polymer capsules. Angew Chem Int Ed 2009;48:4359-4362
33. Jo SM, Lee HY, Kim JC. Glucose-Sensitive Liposomes incorporating hydrophobically modified glucose oxidase. Lipids 2008;43:937-943
34. Huysmans G, Ranquin A, Wyns L, et al. Encapsulation of therapeutic nucleoside hydrolase in functionalised nanocapsules. J Control Release 2005;102:171-179
35. Yoshimoto M, Wang S, Fukunaga K, et al. Novel immobilized liposomal glucose oxidase system using the channel protein OmpF and catalase. Biotechnol Bioeng 2005;90(2):231-238
36. Parmar MM, Edwards K, Madden TD. Incorporation of bacterial membrane proteins into liposomes: factors influencing protein reconstitution. Biochim Biophys Acta 1999;1421:77-90
37. Jayanna PK, Torchilin VP, Petrenko VA. Liposomes targeted by fusion phage proteins. Nanomed Nanotechnol Biol Med 2009;5:83-89
38. Peer D, Karp JM, Hong S, et al. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2007;2:751-760
39. Boddapati SV, D'Souza GGM, Erdogan S, et al. Organelle-targeted nanocarriers: Specific delivery of liposomal ceramide to mitochondria enhances its cytotoxicity in vitro and in vivo. Nano Lett 2008;8(8):2559-2563
40. Stolnik S, Shakesheff K. Formulations for delivery of therapeutic proteins. Biotechnol Lett 2009;31:1-11
41. Onaca O, Enea R, Hughes DW, Meier W. Stimuli-responsive polymersomes as nanocarriers for drug and gene delivery. Macromol Biosci 2009;9:129-139
42. Ahmed F, Discher DE. Self-porating polymersomes of PEG-PLA and PEG-PCL - hydrolysis-triggered controlled release vesicles. J Control Release 2004;96:37-53
43. Ciofani G, Cascone MG, Serino LP, Lazzeri L. Urease loaded alginate microspheres for blood purification. J Microencapsulation 2008;25(8):569-576
44. Sivadas N, O'Rourke D, Tobin A, et al. A comparative study of a range of polymeric microspheres as potential carriers for the inhalation of proteins. Int J Pharm 2008;358:159-167
45. Giteau A, Venier-Julienne MC, Marchal S, et al. Reversible protein precipitation to ensure stability during encapsulation within PLGA microspheres. Eur J Pharm Biopharm 2008;70:127-136
46. Zhou S, Liao X, Li X. Poly-D, L-lactide-co-poly(ethylene glycol) microspheres as potential vaccine delivery systems. J Control Release 2003;86:195-205
47. Kawaguchi H, Fujimoto K, Saito M, et al. Preparation and modification of monodisperse hydrogel microspheres. Polym Int 1993;30:225-231
48. Tamber H, Johansen P, Merkle HP, Gander B. Formulation aspects of biodegradable polymeric microspheres for antigen delivery. Adv Drug Deliv Rev 2004;57:357-376
49. Kim BS, Oh JM, Hyun H, et al. Insulin-loaded microcapsules for in vivo delivery. Mol Pharmacol 2009;6(2):353-365
50. Ghassemi AH, Steenbergen MJV, Talsma H, et al. Preparation and characterization of protein loaded microspheres based on a hydroxylated aliphatic polyester, poly (lactic-co-hydroxymethyl glycolic acid). J Control Release 2009;138(1):57-63
51. Houchin ML, Topp EM. Chemical degradation of peptides and proteins in PLGA: A review of reactions and mechanisms. J Pharm 2008;97:2395-2404
52. Coccoli V, Luciani A, Orsi S, et al. Engineering of PCL microcarriers to modulate protein encapsulation capability and release kinetic. J Mater Sci Mater Med 2008;19:1703-1711
53. Gopferich A, Tessmar J. Polyanhydride degradation and erosion. Adv Drug Deliv Rev 2002;54:911-931
54. Sun L, Zhou S, Wang W, et al. Preparation and characterization of protein-loaded polyanhydride microspheres. J Mater Sci Mater Med 2009;20(10):2035-2042
55. Celik O, Akbuga J. Preparation of superoxide dismutase loaded chitosan microspheres: characterization and release studies. Eur J Pharm Biopharm 2007;66:42-47
56. Zauner W, Farrow NA, Haines AMR. In vitro uptake of polystyrene microspheres: effect of particle size, cell line and cell density. J Control Release 2001;71:39-51
57. Nishiyama N, Jang WD, Kataoka K. Supramolecular nanocarriers integrated with dendrimers encapsulating photosensitizers for effective photodynamic therapy and photochemical gene delivery. New J Chem 2007;31:1074-1082
58. Hales K, Pochan DJ. Using polyelectrolyte block copolymers to tune nanostructure assembly. Curr Opin Colloid Interface Sci 2006;11(6):330-336
59. Voets IK, Keizer AD, Stuart MAC. Complex coacervate core micelles. Adv Colloid Interface Sci 2009;147-148:300-318
60. Haidar ZS, Hamdy RC, Tabrizian M. Protein release kinetics for core-shell hybrid nanoparticles based on the layer-by-layer assembly of alginate and chitosan on liposomes. Biomaterials 2008;29:1207-1215
61. Akamatsu K, Yamaguchi T. Novel Preparation Method for obtaining pH-responsive core-shell microcapsule reactors. Ind Eng Chem Res 2007;46(1):124-130
62. Simone EA, Dziubla TD, Arguiri E, et al. Loading PEG-Catalase into filamentous and spherical polymer nanocarriers. Pharm Res 2009;26(1):250-260
63. Christian DA, Cai S, Bowen DM, et al. Polymersome carriers: From self-assembly to siRNA and protein therapeutics. Eur J Pharm Biopharm 2009;71(3):463-474
64. Uchegbu IF. Pharmaceutical nanotechnology: polymeric vesicles for drug and gene delivery. Expert Opin Drug Deliv 2006;3(5):629-640
65. Peppas NA, Hilt JZ, Khademhosseini A, Langer R. Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv Mater 2006;18:1345-1360
66. Yang Z, Xu B. Supramolecular hydrogels based on biofunctional nanofibers of self-assembled small molecules. J Mater Chem 2007;17:2385-2393 (Pubitemid 46884065)
67. Watari F, Takashi N, Yokoyama A, et al. Physical size effects material nanosizing effect on living organisms: non-specific. J R Soc Interface 2009;6:S371-88
68. Singh R, Lillard JW Jr. Nanoparticle-based targeted drug delivery. Exp Mol Pathol 2009;86(3):215-223
69. Hasadsri L, Kreuter J, Hattori H, et al. Functional protein delivery into neurons using polymeric nanoparticles. J Biol Chem 2009;284(11):6972-6981
70. Reddy MK, Wu L, Kou W, et al. Superoxide dismutase-loaded PLGA nanoparticles protect cultured human neurons under oxidative stress. Appl Biochem Biotechnol 2008;151:565-577
71. Reddy MK, Labhasetwar V. Nanoparticle-mediated delivery of superoxide dismutase to the brain: an effective strategy to reduce ischemia-reperfusion injury. J FASEB 2009;23:1384-1395
72. Lee S, Yang SC, Heffernan MJ, et al. Polyketal Microparticles: a new delivery vehicle for superoxide dismutase. Bioconjugate Chem 2007;18:4-7
73. Garnacho C, Dhami R, Simone E, et al. Delivery of acid sphingomyelinase in normal and Niemann-Pick disease mice using intercellular adhesion molecule-1-targeted polymer nanocarriers. J Pharmacol Exp Ther 2008;325(2):400-408
74. Dziubla TD, Shuvaev VV, Hong NK, et al. Endothelial targeting of semi-permeable polymer nanocarriers for enzyme therapies. Biomaterials 2008;29:215-227
75. Rosler A, Vandermeulen GWM, Klok HA. Advanced drug delivery devices via self-assembly of amphiphilic block copolymers. Adv Drug Deliv Rev 2001;53(1):95-108
76. Croy SR, Kwon GS. Polymeric micelles for drug delivery. Curr Pharm Design 2006;12:4669-4684
77. Huh KM, Lee SC, Cho YW, et al. Hydrotropic polymer micelle system for delivery of paclitaxel. J Control Release 2005;101(1-3):59-68
78. Lee JS, Bae JW, Joung YK, et al. Controlled dual release of basic fibroblast growth factor and indomethacin from heparin-conjugated polymeric micelle. Int J Pharm 2008;346(1-2):57-63
79. Miller AC, Bershteyn A, Tan W, et al. Block copolymer micelles as nanocontainers for controlled release of proteins from biocompatible oil phases. Biomacromolecules 2009;10(4):732-741
80. Jones MC, Tewari P, Blei C, et al. Self-Assembled nanocages for hydrophilic guest molecules. J Am Chem Soc 2006;128(45):14599-14605
81. Rapoport N. Physical stimuli-responsive polymeric micelles for anti-cancer drug delivery. Prog Polym Sci 2007;32:962-990
82. Ganta S, Devalapally H, Shahiwala A, Amiji M. A review of stimuli-responsive nanocarriers for drug and gene delivery. J Control Release 2008;126:187-204
83. Perez C, Castellanos IJ, Costantino HR, et al. Recent trends in stabilizing protein structure upon encapsulation and release from bioerodible polymers. J Pharm Pharmacol 2002;54(3):301-313
84. Wittemann A, Azzam T, Eisenberg A. Biocompatible polymer vesicles from biamphiphilic triblock copolymers and their interaction with bovine serum albumin. Langmuir 2007;23(4):2224-2230
85. Arifin DR, Palmer AF. Polymersome encapsulated hemoglobin: A novel type of oxygen carrier. Biomacromol 2005;6:2172-2181
86. Palivan C, Vebert C, Axthelm F, Meier W. Responsive self-assembled nanostructures. Nanotechnol Biol Med 2007;32(1):467-492
87. Robbins GP, Jimbo M, Swift J, et al. Photoinitiated destruction of composite porphyrin-protein polymersomes. J Am Chem Soc 2009;131:3872-3874
88. Dror Y, Kuhn J, Avrahami R, Zussman E. Encapsulation of enzymes in biodegradable tubular structures. Macromolecules 2008;41:4187-4192
89. Chen Q, Schonherr H, Vancso GJ. Block-copolymer vesicles as nanoreactors for enzymatic reactions. Small 2009;5:36-46
90. Napoli A, Boerakker MJ, Tirelli N, et al. Hubbell, Glucose-oxidase based self-destructing polymeric vesicles. Langmuir 2004;20:3487-3491
91. Axthelm F, Casse O, Koppenol WH, et al. Antioxidant nanoreactor based on superoxide dismutase encapsulated in superoxide-permeable vesicles. J Phy Chem B 2008;112:8211-8217
92. Vriezema DM, Hoogboom J, Velonia K, et al. Vesicles and polymerized vesicles from thiophene-containing rod-coil block copolymers. Angew Chem Int Ed 2003;42:772-776
93. Lvov Y, Antipov AA, Mamedov A, et al. Urease encapsulation in nanoorganized microshells. Nano Lett 2001;1:125-128
94. Nardin C, Widmer J, Winterhalter M, Meier W. Amphiphilic block copolymer nanocontainers as bioreactors. Eur Phys J E 2001;4:403-410
95. Ranquin A, Versees W, Meier W, et al. Therapeutic nanoreactors: combining chemistry and biology in a novel triblock copolymer drug delivery system. Nano Lett 2005;5:2220-2224
96. Nallani M, Benito S, Onaca O, et al. A nanocompartment system (Synthosome) designed for biotechnological applications. J Biotechnol 2006;123:50-59
97. Kumar M, Grzelakowski M, Zilles J, et al. Highly permeable polymeric membranes based on the incorporation of the functional water channel protein Aquaporin Z. Proc Nat Acad Sci USA 2007;104:20719-20724
98. Graff A, Sauer M, Gelder PV, Meier W. Virus assisted loading of polymer nanocontainer. Proc Nat Acad Sci USA 2002;99:5064-5068
99. Broz P, Driamov S, Ziegler J, et al. Toward intelligent nanosize bioreactors: A pH-switchable, channel-equipped, functional polymer nanocontainer. Nano Lett 2006;6(10):2349-2353
100. Vriezema DM, Garcia PML, Oltra NS, et al. Positional assembly of enzymes in polymersome nanoreactors for cascade reactions. Angew Chem Int Ed 2007;46:7378-7382
101. Kreft O, Prevot M, Mohwald H, Sukhorukov GB. Shell-in-shell microcapsules: A novel tool for integrated, spatially confined enzymatic reactions. Angew Chem Int Ed 2007;46:5605-5608
102. Kuiper SM, Nallani M, Vriezema DM, et al. Enzymes containing porous polymersomes as nano reaction vessels for cascade reactions. Org Biomol Chem 2008;6:4315-4318
103. Onaca O, Sarkar P, Roccatano D, et al. Functionalized nanocompartments (Synthosomes) with a reduction-triggered release system. Angew Chem Int Ed 2008;47:7029-7031
104. Comellas-Aragones M, Engelkamp H, Claessen VI, et al. A virus-based single-enzyme nanoreactor. Nat Nanotechnol 2007;2:635-639
105. Escosura ADL, Nolte RJM, Cornelissen JJLM. Viruses and protein cages as nanocontainers and nanoreactors. J Mater Chem 2009;19:2274-2278
106. Beduneau A, Saulnier P, Benoit JP. Active targeting of brain tumors using nanocarriers. Biomaterials 2007;28:4947-4967
107. Song CK, Jung SH, Kim DD, et al. Disaccharide-modified liposomes and their in vitro intracellular uptake. Int J Pharm 2009;380:161-169
108. Garg A, Tisdale AW, Haidari E, Kokkoli E. Targeting colon cancer cells using PEGylated liposomes modified with a fibronectin-mimetic peptide. Int J Pharm 2009;366:201-210
109. Mustata RC, Grigorescu A, Petrescu SM. Encapsulated cargo internalized by fusogenic liposomes partially overlaps the endoplasmic reticulum. J Cell Mol Med 2009, doi: 10.1111/ j.1582-4934.2009.00724
110. Oh IK, Mok H, Park TG. Folate immobilized and PEGylated adenovirus for retargeting to tumor cells. Bioconjugate Chem 2006;17(3):721-727
111. Lee KY, Yuk SH. Polymeric protein delivery systems. Prog Polym Sci 2007;32:669-697
112. Khandare JJ, Minko T. Antibodies and peptides in cancer therapy. Crit Rev Ther Drug Carrier Syst 2006;23:401-436
113. Garnacho C, Albelda SM, Muzykantov VR, Muro S. Differential intra-endothelial delivery of polymer nanocarriers targeted to distinct PECAM-1 epitopes. J Control Release 2008;130:226-233
114. Kommareddy S, Tiwari SB, Amiji MM. Long-circulating polymeric nanovectors for tumor-selective gene delivery. Technol Cancer Res Treat 2005;4(6):615-625
115. Chen F, Zhang ZR, Yuan F, et al. In vitro and in vivo study of N-trimethyl chitosan nanoparticles for oral protein delivery. Int J Pharm 2008;349:226-233
116. Colonna C, Conti B, Perugini P, et al. Ex vivo evaluation of prolidase loaded chitosan nanoparticles for the enzyme replacement therapy. Eur J Pharm Biopharm 2008;70:58-65
117. Gan Q, Wang T. Chitosan nanoparticle as protein delivery carrier-Systematic examination of fabrication conditions for efficient loading and release. Colloids Surf B 2007;59:24-34
118. Won YW, Kim YH. Recombinant human gelatin nanoparticles as a protein drug carrier. J Control Release 2008;127:154-161
119. Bachelder EM, Beaudette TT, Broaders KE, Paramonov SE. Acid-degradable polyurethane particles for protein-based vaccines: biological evaluation and in vitro analysis of particle degradation products. Mol Pharmacol 2008;5(5):876-884
120. Dziubla TD, Karim A, Muzykantov VR. Polymer nanocarriers protecting active enzyme cargo against proteolysis. J Control Release 2005;102:427-439
121. Ghoroghchian PP, Frail PR, Susumu K, et al. Broad spectral domain fluorescence wavelength modulation of visible and near-infrared emissive polymersomes. J Am Chem Soc 2005;127:15388-15390
122. Ben-Haim N, Broz P, Marsch S, et al. Cell-Specific Integration of artificial organelles based on functionalized polymer vesicles. Nano Lett 2008;8:1368-1373
123. Mercado AE, He X, Xu W, Jabbari E. The release characteristics of a model protein from self-assembled succinimide-terminated poly (lactide-co-glycolide ethylene oxide fumarate) Nanoparticles. Nanotechnology 2008;19:325609-325620
124. Piras AM, Dessy A, Chiellini F, et al. Polymeric nanoparticles for hemoglobin-based oxygen carriers. Biochim Biophys Acta 2008;1784:1454-1461
125. Standley SM, Mende I, Goh SL, et al. Incorporation of CpG oligonucleotide ligand into protein-loaded particle vaccines promotes antigen-specific CD8 T-cell immunity. Bioconjugate Chem 2007;18:77-83