Can polymeric vesicles that confine enzymatic reactions act as simplified organelles?

FEBS Letters

Volumn 585, Issue 11, 2011, Pages 1699-1706

  Tanner, Pascal ^a   Egli, Stefan ^a   Balasubramanian, Vimalkumar ^a   Onaca, Ozana ^a   Palivan, Cornelia G ^a   Meier, Wolfgang ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Artificial organelle; Cell uptake; Enzyme activity; Nanoreactor; Requirement; Self assembly

Indexed keywords

2 METHACRYLOYLOXYETHYLPHOSPHORYLCHOLINE; AQUAPORIN; COPOLYMER; DIMETICONE; OUTER MEMBRANE PROTEIN F; POLY (2 (METHYCRYLOYLOXY)ETHYL PHOSPHORYLCHOLINE) CO POLY (2 DIISOPROPYLAMINO)ETHYL METHYCRYLATE COPOLYMER; POLY (2 METHYL 2 OXAZOLINE); POLY (G BENZYL GLUTAMATE) COPOLYMER; POLY(ETHYLENE GLYCOL) CO POLY (2 (DIISOPROPYLAMINO)ETHYL METHACRYLATE) COPOLYMER; POLY(ETHYLENE OXIDE) POLY (2 (DIISOPROPYLAMINO)ETHYL METHYCRYLATE) POLY(DIMETHYL ACRYLAMIDE) COPOLYMER; POLYMER; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ARTIFICIAL CELL; BIOCOMPATIBILITY; CATALYSIS; CELL ORGANELLE; DRUG DELIVERY SYSTEM; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME REPLACEMENT; ENZYME SUBSTRATE; HYDROPHILICITY; LIPID MEMBRANE; LIPID VESICLE; NANOENCAPSULATION; POLYMERIZATION; POROSITY; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; TOXICITY TESTING;

ANIMALS; BIOMIMETICS; ENZYMES; MEMBRANES, ARTIFICIAL; ORGANELLES; POLYMERS;

EID: 79957572409     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2011.05.003     Document Type: Review

References (87)

1. M. Antonietti, and S. Foerster Vesicles and liposomes: a self-assembly principle beyond lipids Adv. Mater. 15 2003 1323 1333
2. D.E. Discher, and F. Ahmed Polymersomes Annu. Rev. Biomed. Eng. 8 2006 323 341 (Pubitemid 44314820)
3. D.E. Discher, and A. Eisenberg Polymer vesicles Science 297 2002 967 973 (Pubitemid 34856022)
4. Malinova, V., Belegrinou, S., Bruyn Ouboter, D.D. and Meier, W. (2009) Biomimetic Block Copolymer Membranes in Polymer Membranes/Biomembranes. Springer, Berlin/Heidelberg, pp. 113-166.
5. V. Balasubramanian, O. Onaca, R. Enea, D.W. Hughes, and C.G. Palivan Protein delivery: from conventional drug delivery carriers to polymeric nanoreactors Expert Opinion Drug Delivery 7 2010 63 78
6. P. Baumann, P. Tanner, O. Onaca, and C.G. Palivan Bio-decorated polymer membranes: a new approach in diagnostics and therapeutics Polymers 3 2011 173 192
7. W. Meier, C. Nardin, and M. Winterhalter Reconstitution of channel proteins in (polymerized) ABA triblock copolymer membranes Ang. Chem. Int. Ed. 39 2000 4599 4602 (Pubitemid 32059118)
8. A. Napoli, M.J. Boerakker, N. Tirelli, R.J.M. Nolte, N.A.J.M. Sommerdijk, and J.A. Hubbell Glucose oxidase-based self-destructing polymeric vesicles Langmuir 20 2004 3487 3491
9. C. Nardin, S. Thoeni, J. Widmer, M. Winterhalter, and W. Meier Nanoreactors based on (polymerized) ABA-triblock copolymer vesicles Chem. Commun. (Cambridge, UK) 1433 2000 1434
10. D.M. Vriezema, M.C. Aragones, J.A.A.W. Elemans, J.J.L.M. Cornelissen, A.E. Rowan, and R.J.M. Nolte Self-assembled nanoreactors Chem. Rev. (Washington, DC, US) 105 2005 1445 1489 (Pubitemid 40596870)
11. D.M. Vriezema, P.M.L. Garcia, N.S. Oltra, N.S. Natzakis, S.M. Kuiper, R.J.M. Nolte, A.E. Rowan, and J.C.M. van Hest Positional assembly of enzymes in polymersome nanoreactors for cascade reactions Angew. Chem. 46 2007 7378 7382 (Pubitemid 47556160)
12. D.J. Adams, C. Kitchen, S. Adams, S. Furzeland, D. Atkins, P. Schuetz, C.M. Fernyhough, N. Tzokova, A.J. Ryan, and M.F. Butler On the mechanism of formation of vesicles from poly(ethylene oxide)-block-poly(caprolactone) copolymers Soft Matt. 5 2009 3086 3096
13. K.E. Gebhardt, S. Ahn, G. Venkatachalam, and D.A. Savin Role of secondary structure changes on the morphology of polypeptide-based block copolymer vesicles J. Colloid Interf. Sci. 317 2008 70 76 (Pubitemid 350088810)
14. C. Schatz, S. Louguet, J.-F. Le Meins, and S. Lecommandoux Polysaccharide-block-polypeptide copolymer vesicles: towards synthetic viral capsids Angew. Chem. 48 2009 2572 2575
15. K.K. Upadhyay, J.F. Le Meins, A. Misra, P. Voisin, V. Bouchaud, E. Ibarboure, C. Schatz, and S. Lecommandoux Biomimetic Doxorubicin Loaded Polymersomes from Hyaluronan-block-Poly(gamma-benzyl glutamate) Copolymers Biomacromolecules 10 2009 2802 2808
16. D.J. Adams, D. Atkins, A.I. Cooper, S. Furzeland, A. Trewin, and I. Young Vesicles from peptidic side-chain polymers synthesized by atom transfer radical polymerization Biomacromolecules 9 2008 2997 3003
17. E.G. Bellomo, M.D. Wyrsta, L. Pakstis, D.J. Pochan, and T.J. Deming Stimuli-responsive polypeptide vesicles by conformation-specific assembly Nat. Mater. 3 2004 244 248
18. H. Schlaad, L. You, R. Sigel, B. Smarsly, M. Heydenreich, A. Mantion, and A. MaAiA Glycopolymer vesicles with an asymmetric membrane Chem. Commun. 1478 2009 1480
19. L. Lin, Z. Yan, J. Gu, Y. Zhang, Z. Feng, and Y. Yu UV-responsive behavior of azopyridine-containing diblock copolymeric vesicles: photoinduced fusion, disintegration and rearrangement Macromol. Rapid Commun. 30 2009 1089 1093
20. E. Mabrouk, D. Cuvelier, F. Brochard-Wyart, P. Nassoy, and M.H. Li Bursting of sensitive polymersomes induced by curling Proc. Natl. Acad. Sci. USA 106 2009 7294 7298
21. S. Yu, T. Azzam, I. Rouiller, and A. Eisenberg "Breathing" Vesicles J. Am. Chem. Soc. 131 2009 10557 10566
22. X. Li, I.V. Pivkin, H. Liang, and G.E. Karniadakis Shape transformations of membrane vesicles from amphiphilic triblock copolymers: a dissipative particle dynamics simulation study Macromolecules 42 2009 3195 3200
23. F. Liu, and A. Eisenberg Preparation and pH triggered inversion of vesicles from poly(acrylic acid)-block-polystyrene-block-poly(4-vinyl pyridine) J. Am. Chem. Soc. 125 2003 15059 15064 (Pubitemid 37509669)
24. R. Stoenescu, and W. Meier Vesicles with asymmetric membranes from amphiphilic ABC triblock copolymers Chem. Commun. 3016 2002 3017
25. F. Li, S. Prevost, R. Schweins, A.T.M. Marcelis, F.A.M. Leermakers, M.A. Cohen Stuart, and E.J.R. Sudholter Small monodisperse unilamellar vesicles from binary copolymer mixtures Soft Matter 5 2009 4169 4172
26. K.P. Davis, T.P. Lodger, and F.S. Bates Vesicle membrane thickness in aqueous dispersions of block copolymer blends 41 2008 8289 8291
27. A.V. Korobko, C. Backendorf, and d.M.J.R.C. van Plasmid DNA encapsulation within cationic diblock copolymer vesicles for gene delivery J. Phys. Chem. B 110 2006 14550 14556 (Pubitemid 44325028)
28. K. Schillen, K. Bryskhe, and Y.S. Mel'nikova Vesicles formed from a poly(ethylene oxide)-poly(propylene oxide)-poly(ethylene oxide) triblock copolymer in dilute aqueous solution Macromolecules 32 1999 6885 6888
29. R. Dimova, U. Seifert, B. Pouligny, S. Forster, and H.G. Dobereiner Hyperviscous diblock copolymer vesicles Eur. Phys. J. E 7 2002 241 250 (Pubitemid 36185052)
30. Le Meins, J.F., Sandre, O. and Lecommandoux, S. (2011) Recent trends in the tuning of polymersomes' membrane properties. Eur. Phys. J. E, 34.
31. M. Guo, M. Jiang, and G. Zhang Surface modification of polymeric vesicles via host-guest inclusion complexation Langmuir 24 2008 10583 10586
32. D.A. Hammer, G.P. Robbins, J.B. Haun, J.J. Lin, W. Qi, L.A. Smith, P.P. Ghoroghchian, M.J. Therien, and F.S. Bates Leuko-polymersomes Faraday Discuss. 139 2008 129 141
33. R. Nehring, C.G. Palivan, O. Casse, P. Tanner, J. Tuxen, and W. Meier Amphiphilic diblock copolymers for molecular recognition: metal-nitrilotriacetic acid functionalized vesicles Langmuir 25 2008 1122 1130
34. R. Nehring, C.G. Palivan, S. Moreno-Flores, A. Mantion, P. Tanner, J.L. Toca-Herrera, A. Thuenemann, and W. Meier Protein decorated membranes by specific molecular interactions Soft Matter 6 2010 2815 2824
35. S.F.M. Van Dongen, W.P.R. Verdurmen, R.J.R.W. Peters, R.J.M. Nolte, R. Brock, and J.C.M. Van Hest Cellular integration of an enzyme-loaded polymersome nanoreactor Angew. Chem. 49 2010 7213 7216
36. J. Gaspard, M.S. Hahn, and J.A. Silas Polymerization of hydrogels inside self-assembled block copolymer vesicles Langmuir 25 2009 12878 12884
37. F. Axthelm, O. Casse, H. Koppenol Willem, T. Nauser, W. Meier, and G. Palivan Cornelia Antioxidant nanoreactor based on superoxide dismutase encapsulated in superoxide-permeable vesicles J. Phys. Chem. B 112 2008 8211 8217
38. M. Kumar, M. Grzelakowski, J. Zilles, M. Clark, and W. Meier Highly permeable polymeric membranes based on the incorporation of the functional water channel protein Aquaporin Z Proc. Natl. Acad. Sci. USA 1 2007 1 6 6 pp
39. D. Ho, B. Chu, H. Lee, and C.D. Montemagno Protein-driven energy transduction across polymeric biomembranes Nanotechnology 15 2004 1084 1094
40. A. Ranquin, W. Versees, W. Meier, J. Steyaert, and P. Van Gelder Therapeutic nanoreactors: combining chemistry and biology in a novel triblock copolymer drug delivery system Nano Lett. 5 2005 2220 2224 (Pubitemid 41698942)
41. V. Pata, and N. Dan The effect of chain length on protein solubilization in polymer-based vesicles (polymersomes) Biophys. J. 85 2003 2111 2118 (Pubitemid 37210765)
42. M. Grzelakowski, O. Onaca, P. Rigler, M. Kumar, and W. Meier Immobilized protein-polymer nanoreactors Small 5 2009 2545 2548
43. A. Graff, C. Fraysse-Ailhas, C.G. Palivan, M. Grzelakowski, T. Friedrich, C. Vebert, G. Gescheidt, and W. Meier Amphiphilic copolymer membranes promote NADH:ubiquinone oxidoreductase activity: towards an electron-transfer nanodevice Macromol. Chem. Phys. 211 2010 229 238
44. A. Graff, M. Sauer, P. Van Gelder, and W. Meier Virus-assisted loading of polymer nanocontainer Proc. Natl. Acad. Sci. USA 99 2002 5064 5068 (Pubitemid 34411504)
45. N. Ben-Haim, P. Broz, S. Marsch, W. Meier, and P. Hunziker Cell-specific integration of artificial organelles based on functionalized polymer vesicles Nano Lett. 8 2008 1368 1373
46. Q. Chen, H. Schoenherr, and G.J. Vancso Block-copolymer vesicles as nanoreactors for enzymatic reactions Small 5 2009 1436 1445
47. C. Nardin, and W. Meier Hybrid materials from amphiphilic block copolymers and membrane proteins Rev. Mol. Biotechnol. 90 2002 17 26 (Pubitemid 34179587)
48. P. Broz, S. Driamov, J. Ziegler, N. Ben-Haim, S. Marsch, W. Meier, and P. Hunziker Toward intelligent nanosize bioreactors: a ph-switchable, channel-equipped, functional polymer nanocontainer Nano Lett. 6 2006 2349 2353 (Pubitemid 44663830)
49. M. Nallani, S. Benito, O. Onaca, A. Graff, M. Lindemann, M. Winterhalter, W. Meier, and U. Schwaneberg A nanocompartment system (Synthosome) designed for biotechnological applications J. Biotechnol. 123 2006 50 59
50. C. De Vocht, A. Ranquin, R. Willaert, G.J.A. Van, T. Vanhaecke, V. Rogiers, W. Versees, G.P. Van, and J. Steyaert Assessment of stability, toxicity and immunogenicity of new polymeric nanoreactors for use in enzyme replacement therapy of mitochondrial neurogastrointestinal encephalomyopathy J. Contr. Rel. 137 2009 246 254
51. P. Tanner, O. Onaca, V. Balasubramanian, W. Meier, and C.G. Palivan Enzymatic cascade reactions inside polymeric nanocontainers: a means to combat oxidative stress Chem. Eur. J. 17 2011 4552 4560
52. S.F.M. van Dongen, M. Nallani, J.J.L.M. Cornelissen, R.J.M. Nolte, and J.C.M. van Hest A three-enzyme cascade reaction through positional assembly of enzymes in a polymersome nanoreactor Chem. Eur. J. 15 2009 1107 1114
53. A. Graff, M. Winterhalter, and W. Meier Nanoreactors from polymer-stabilized liposomes Langmuir 17 2001 919 923 (Pubitemid 32873072)
54. C. Nardin, J. Widmer, M. Winterhalter, and W. Meier Amphiphilic block copolymer nanocontainers as bioreactors Eur. Phys. J. E 4 2001 403 410
55. P. Dalhaimer, F.S. Bates, H. Aranda-Espinoza, and D. Discher Synthetic cell elements from block copolymers - hydrodynamic aspects C. R. Phys. 4 2003 251 258 (Pubitemid 36623994)
56. J.R. Howse, R.A.L. Jones, G. Battaglia, R.E. Ducker, G.J. Leggett, and A.J. Ryan Templated formation of giant polymer vesicles with controlled size distributions Nat. Mater. 8 2009 507 511
57. A. Rank, S. Hauschild, S. Forster, and R. Schubert Preparation of monodisperse block copolymer vesicles via a thermotropic cylinder-vesicle transition Langmuir 25 2009 1337 1344
58. L. Ma, and A. Eisenberg Relationship between wall thickness and size in block copolymer vesicles Langmuir 25 2009 13730 13736
59. K. Kita-Tokarczyk, J. Grumelard, T. Haefele, and W. Meier Block copolymer vesicles-using concepts from polymer chemistry to mimic biomembranes Polymer 46 2005 3540 3563 (Pubitemid 40560121)
60. J.C.M. Lee, H. Bermudez, B.M. Discher, M.A. Sheehan, Y.-Y. Won, F.S. Bates, and D.E. Discher Preparation, stability, and in vitro performance of vesicles made with diblock copolymers Biotechnol. Bioeng. 73 2001 135 145 (Pubitemid 32291402)
61. O.P. Tiourina, A.A. Antipov, G.B. Sukhorukov, N.I. Larionova, Y. Lvov, and H. Möhwald Entrapment of α-Chymotrypsin into Hollow Polyelectrolyte Microcapsules Macromol. Biosci. 1 2001 209 214 (Pubitemid 33641089)
62. O. Onaca, D.W. Hughes, V. Balasubramanian, M. Grzelakowski, W. Meier, and C.G. Palivan SOD antioxidant nanoreactors: influence of block copolymer composition on the nanoreactor efficiency Macromol. Biosci. 10 2010 531 538
63. J.Y. Wong, J.B. Leach, and X.Q. Brown Balance of chemistry, topography, and mechanics at the cell-biomaterial interface. Issues and challenges for assessing the role of substrate mechanics on cell response Surf. Sci. 570 2004 119 133
64. H. Lomas, M. Massignani, K.A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S.P. Armes, A.L. Lewis, and G. Battaglia Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery Faraday Discuss. 139 2008 143 159
65. M. Massignani, H. Lomas, and G. Battaglia Polymersomes: a synthetic biological approach to encapsulation and delivery Adv. Polym. Sci. 229 2010 115 154
66. M. Massignani, C. LoPresti, A. Blanazs, J. Madsen, S.P. Armes, A.L. Lewis, and G. Battaglia Controlling cellular uptake by surface chemistry, size, and surface topology at the nanoscale Small 5 2009 2424 2432
67. V.D. Awasthi, D. Garcia, R. Klipper, B.A. Goins, and W.T. Phillips Neutral and anionic liposome-encapsulated hemoglobin: effect of postinserted poly(ethylene glycol)-distearoylphosphatidylethanolamine on distribution and circulation kinetics J. Pharmacol. Exp. Ther. 309 2004 241 248 (Pubitemid 38393136)
68. K. Furumoto, S. Nagayama, K.-i. Ogawara, Y. Takakura, M. Hashida, K. Higaki, and T. Kimura Hepatic uptake of negatively charged particles in rats: possible involvement of serum proteins in recognition by scavenger receptor J. Contr. Rel. 97 2004 133 141 (Pubitemid 38624516)
69. Y. Yamamoto, Y. Nagasaki, Y. Kato, Y. Sugiyama, and K. Kataoka Long-circulating poly(ethylene glycol)-poly(-lactide) block copolymer micelles with modulated surface charge J. Contr. Rel. 77 2001 27 38 (Pubitemid 33022613)
70. C. Murdoch, K.J. Reeves, V. Hearnden, H. Colley, M. Massignani, I. Canton, J. Madsen, A. Blanazs, S.P. Armes, A.L. Lewis, S. MacNeil, N.J. Brown, M.H. Thornhill, and G. Battaglia Internalization and biodistribution of polymersomes into oral squamous cell carcinoma cells in vitro and in vivo Nanomedicine-Uk 5 2010 1025 1036
71. D.A. Christian, O.B. Garbuzenko, T. Minko, and D.E. Discher Polymer vesicles with a red cell-like surface charge: microvascular imaging and in vivo tracking with near-infrared fluorescence Macromol. Rapid Commun. 31 2010 135 141
72. D.E. Owens III, and N.A. Peppas Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles Int. J. Pharm. 307 2006 93 102 (Pubitemid 41773257)
73. C. Fang, B. Shi, Y.-Y. Pei, M.-H. Hong, J. Wu, and H.-Z. Chen In vivo tumor targeting of tumor necrosis factor-[alpha]-loaded stealth nanoparticles: effect of MePEG molecular weight and particle size Eur. J. Pharm. Sci. 27 2006 27 36 (Pubitemid 41728252)
74. H. Lomas, I. Canton, S. MacNeil, J. Du, S.P. Armes, A.J. Ryan, A.L. Lewis, and G. Battaglia Biomimetic pH sensitive polymersomes for efficient DNA encapsulation and delivery Adv. Mater. (Weinheim, Ger) 19 2007 4238 4243 (Pubitemid 350254804)
75. Balasubramanian, V., Onaca, O., Ezhevskaya, M., Van Doorslaer, S., Sivasankaran, B. & Palivan Cornelia, G. A surprising system: polymeric nanoreactors containing a mimic with dual-enzyme activity-in press, Soft Matter, DOI:10.1039/C1SM05215B.
76. I.A. Khalil, K. Kogure, H. Akita, and H. Harashima Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery Pharmacol. Rev. 58 2006 32 45
77. E. Jan, S.J. Byrne, M. Cuddihy, A.M. Davies, Y. Volkov, Y.K. Gun'ko, and N.A. Kotov High-content screening as a universal tool for fingerprinting of cytotoxicity of nanoparticles ACS Nano 2 2008 928 938
78. A.N. Zelikin, A.D. Price, and B. Städler Poly(methacrylic acid) polymer hydrogel capsules: drug carriers, sub-compartmentalized microreactors, artificial organelles Small 6 2010 2201 2207
79. G. Pasparakis, N. Krasnogor, L. Cronin, B.G. Davis, and C. Alexander Controlled polymer synthesis-from biomimicry towards synthetic biology Chem. Soc. Rev. 39 2010 286 300
80. Barnier Quer, C., Robson Marsden, H., Romeijn, S., Zope, H., Kros, A. & Jiskoot, W. (2011) Polymersomes enhance the immunogenicity of influenza subunit vaccine, Polym. Chem. Uk., DOI: 10.1039/c1py00010a.
81. Blanazs, A., Massignani, M., Battaglia, G., Armes, S. P. & Ryan, A. J. (2008) Synthesis of pH-responsive amphiphilic ABC block copolymers: the generation of asymmetric vesicle membranes and their cell uptake kinetics. Abstr. Papers Am. Chem. Soc. 236, 393-POLY.
82. N.A. Christian, M.C. Milone, S.S. Ranka, G.Z. Li, P.R. Frail, K.P. Davis, F.S. Bates, M.J. Therien, P.P. Ghoroghchian, C.H. June, and D.A. Hammer Tat-functionalized near-infrared emissive polymersomes for dendritic cell labeling Bioconjug. Chem. 18 2007 31 40 (Pubitemid 46145992)
83. J.-P.Y. Scheerlinck, and D.L.V. Greenwood Virus-sized vaccine delivery systems Drug Discovery Today 13 2008 882 887
84. P. Broz, S.M. Benito, C. Saw, P. Burger, H. Heider, M. Pfisterer, S. Marsch, W. Meier, and P. Hunziker Cell targeting by a generic receptor-targeted polymer nanocontainer platform J. Contr. Rel. 102 2005 475 488 (Pubitemid 40093767)
85. C.P. O'Neil, T. Suzuki, D. Demurtas, A. Finka, and J.A. Hubbell A novel method for the encapsulation of biomolecules into polymersomes via direct hydration Langmuir 25 2009 9025 9029
86. X. Yang, J.J. Grailer, I.J. Rowland, A. Javadi, S.A. Hurley, V.Z. Matson, D.A. Steeber, and S. Gong Multifunctional stable and pH-responsive polymer vesicles formed by heterofunctional triblock copolymer for targeted anticancer drug delivery and ultrasensitive MR imaging ACS Nano 4 2010 6805 6817
87. S. Egli, H. Schlaad, N. Bruns, and W. Meier Functionalization of block copolymer vesicle surfaces Polymers 3 2011 252 280