Ion-induced cell sheet detachment from standard cell culture surfaces coated with polyelectrolytes

Biomaterials

Volumn 33, Issue 12, 2012, Pages 3421-3427

  Zahn, Raphael ^a   Thomasson, Elsa ^a   Guillaume Gentil, Orane ^a   Vörös, János ^a   Zambelli, Tomaso ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Cell sheet; Layer by layer films; Polyelectrolyte multilayer films; Surface modification; Tissue engineering

Indexed keywords

CELL CULTURE MEDIUMS; CELL SHEET; CELL SHEET ENGINEERING; CELLULAR ADHESION; EXTRACELLULAR MATRICES; HYALURONIC ACIDS; L-LYSINE; LAYER BY LAYER DEPOSITION; LAYER-BY-LAYER FILMS; LOW CONCENTRATIONS; MULTIVALENT IONS; MYOBLASTS; POLYANIONS; POLYCATIONS; POLYELECTROLYTE MOLECULES; POLYELECTROLYTE MULTILAYER; POLYELECTROLYTE MULTILAYER FILMS; REGENERATIVE MEDICINE; STANDARD CELL; VIABLE CELLS;

ADHESION; AMINO ACIDS; ATOMIC FORCE MICROSCOPY; CELL CULTURE; CELLS; ELECTRIC BATTERIES; MULTILAYER FILMS; MULTILAYERS; POLYELECTROLYTES; POLYSTYRENES; SURFACE TREATMENT; TISSUE; TISSUE ENGINEERING;

CELL ENGINEERING;

CARBON; FERROCYANIDE; FIBRONECTIN; GLASS; HYALURONIC ACID; ION; POLYELECTROLYTE; POLYLYSINE; POLYSTYRENE; SILICON DIOXIDE;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL CULTURE; CELL SURFACE; CELL VIABILITY; CONCENTRATION (PARAMETERS); CULTURE MEDIUM; DISSOLUTION; EXTRACELLULAR MATRIX; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; REGENERATIVE MEDICINE;

ANIMALS; CELL ADHESION; CELL LINE; COATED MATERIALS, BIOCOMPATIBLE; ELECTROLYTES; FIBRONECTINS; HYALURONIC ACID; MICE; MYOBLASTS; POLYAMINES; POLYLYSINE; POLYMERS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84857036056     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.01.019     Document Type: Article

References (76)

1. Iler R.K. Multilayers of colloidal particles. J Colloid Interface Sci 1966, 21:569-594.
2. Decher G., Hong J.D., Schmitt J. Buildup of ultrathin multilayer films by a self-assembly process: III. consecutively alternating adsorption of anionic and cationic polyelectrolytes on charged surfaces. Thin Solid Films 1992, 210:831-835.
3. Decher G. Fuzzy nanoassemblies: toward layered polymeric multicomposites. Science 1997, 277:1232-1237.
4. Schlenoff J.B. Retrospective on the future of polyelectrolyte multilayers. Langmuir 2009, 25:14007-14010.
5. Hammond P.T. Engineering materials layer-by-layer: challenges and opportunities in multilayer assembly. AICHE J 2011, 57:2928-2940.
6. Lavalle P., Voegel J.C., Vautier D., Senger B., Schaaf P., Ball V. Dynamic aspects of films prepared by a sequential deposition of species: perspectives for smart and responsive materials. Adv Mater 2011, 23:1191-1221.
7. de Villiers M.M., Otto D.P., Strydom S.J., Lvov Y.M. Introduction to nanocoatings produced by layer-by-layer (LbL) self-assembly. Adv Drug Deliv Rev 2011, 63:701-715.
8. Stuart M.A., Huck W.T., Genzer J., Muller M., Ober C., Stamm M., et al. Emerging applications of stimuli-responsive polymer materials. Nat Mater 2010, 9:101-113.
9. Lu O.Y., Malaisamy R., Bruening M.L. Multilayer polyelectrolyte films as nanofiltration membranes for separating monovalent and divalent cations. J Membr Sci 2008, 310:76-84.
10. Adusumilli M., Bruening M.L. Variation of ion-exchange capacity, zeta potential, and ion-transport selectivities with the number of layers in a multilayer polyelectrolyte film. Langmuir 2009, 25:7478-7485.
11. Tang Z.Y., Wang Y., Podsiadlo P., Kotov N.A. Biomedical applications of layer-by-layer assembly: from biomimetics to tissue engineering. Adv Mater 2007, 19:906.
12. Boudou T., Crouzier T., Ren K., Blin G., Picart C. Multiple functionalities of polyelectrolyte multilayer films: new biomedical applications. Adv Mater 2010, 22:441-467.
13. Pavlukhina S., Sukhishvili S. Polymer assemblies for controlled delivery of bioactive molecules from surfaces. Adv Drug Deliv Rev 2011, 63:822-836.
14. Zelikin A.N. Drug releasing polymer thin films: new era of surface-mediated drug delivery. Acs Nano 2010, 4:2494-2509.
15. De Geest B.G., De Koker S., Sukhorukov G.B., Kreft O., Parak W.J., Skirtach A.G., et al. Polyelectrolyte microcapsules for biomedical applications. Soft Matter 2009, 5:282-291.
16. De Geest B.G., Sanders N.N., Sukhorukov G.B., Demeester J., De Smedt S.C. Release mechanisms for polyelectrolyte capsules. Chem Soc Rev 2007, 36:636-649.
17. Ai H. Layer-by-layer capsules for magnetic resonance imaging and drug delivery. Adv Drug Deliv Rev 2011, 63:772-788.
18. Macdonald M.L., Samuel R.E., Shah N.J., Padera R.F., Beben Y.M., Hammond P.T. Tissue integration of growth factor-eluting layer-by-layer polyelectrolyte multilayer coated implants. Biomaterials 2011, 32:1446-1453.
19. Crouzier T., Fourel L., Boudou T., Albiges-Rizo C., Picart C. Presentation of BMP-2 from a soft biopolymeric film unveils its activity on cell adhesion and migration. Adv Mater 2011, 23:H111-H118.
20. Crouzier T., Szarpak A., Boudou T., Auzely-Velty R., Picart C. Polysaccharide-blend multilayers containing hyaluronan and heparin as a delivery system for rhBMP-2. Small 2010, 6:651-662.
21. Crouzier T., Sailhan F., Becquart P., Guillot R., Logeart-Avramoglou D., Picart C. The performance of BMP-2 loaded TCP/HAP porous ceramics with a polyelectrolyte multilayer film coating. Biomaterials 2011, 32:7543-7554.
22. Wong S.Y., Li Q., Veselinovic J., Kim B.S., Klibanov A.M., Hammond P.T. Bactericidal and virucidal ultrathin films assembled layer by layer from polycationic N-alkylated polyethylenimines and polyanions. Biomaterials 2010, 31:4079-4087.
23. Moskowitz J.S., Blaisse M.R., Samuel R.E., Hsu H.P., Harris M.B., Martin S.D., et al. The effectiveness of the controlled release of gentamicin from polyelectrolyte multilayers in the treatment of staphylococcus aureus infection in a rabbit bone model. Biomaterials 2010, 31:6019-6030.
24. Schmidt D.J., Moskowitz J.S., Hammond P.T. Electrically triggered release of a small molecule drug from a polyelectrolyte multilayer coating. Chem Mater 2010, 22:6416-6425.
25. Flessner R.M., Yu Y., Lynn D.M. Rapid release of plasmid DNA from polyelectrolyte multilayers: a weak poly(acid) approach. Chem Commun 2011, 47:550-552.
26. Garza J.M., Jessel N., Ladam G., Dupray V., Muller S., Stoltz J.F., et al. Polyelectrolyte multilayers and degradable polymer layers as multicompartment films. Langmuir 2005, 21:12372-12377.
27. Berg M.C., Zhai L., Cohen R.E., Rubner M.F. Controlled drug release from porous polyelectrolyte multilayers. Biomacromolecules 2006, 7:357-364.
28. Boulmedais F., Tang C.S., Keller B., Voros J. Controlled electrodissolution of polyelectrolyte multilayers: a platform technology towards the surface-initiated delivery of drugs. Adv Funct Mater 2006, 16:63-70.
29. Guillaume-Gentil O., Graf N., Boulmedais F., Schaaf P., Voros J., Zambelli T. Global and local view on the electrochemically induced degradation of polyelectrolyte multilayers: from dissolution to delamination. Soft Matter 2010, 6:4246-4254.
30. Wood K.C., Zacharia N.S., Schmidt D.J., Wrightman S.N., Andaya B.J., Hammond P.T. Electroactive controlled release thin films. Proc Natl Acad Sci USA 2008, 105:2280-2285.
31. Lynn D.M. Peeling back the layers: controlled erosion and triggered disassembly of multilayered polyelectrolyte thin films. Adv Mater 2007, 19:4118-4130.
32. Kerdjoudj H., Berthelemy N., Boulmedais F., Stoltz J.F., Menu P., Voegel J.C. Multilayered polyelectrolyte films: a tool for arteries and vessel repair. Soft Matter 2010, 6:3722-3734.
33. Guillame-Gentil O., Semenov O., Roca A.S., Groth T., Zahn R., Voros J., et al. Engineering the extracellular environment: strategies for building 2D and 3D cellular structures. Adv Mater 2010, 22:5443-5462.
34. Detzel C.J., Larkin A.L., Rajagopalan P. Polyelectrolyte multilayers in tissue engineering. Tissue Eng Part B Rev 2011, 17:101-113.
35. Guillaume-Gentil O., Akiyama Y., Schuler M., Tang C., Textor M., Yamato M., et al. Polyelectrolyte coatings with a potential for electronic control and cell sheet engineering. Adv Mater 2008, 20:560-565.
36. Guillaume-Gentil O., Semenov O.V., Zisch A.H., Zimmermann R., Voros J., Ehrbar M. pH-controlled recovery of placenta-derived mesenchymal stem cell sheets. Biomaterials 2011, 32:4376-4384.
37. Okano T., Yamada N., Sakai H., Sakurai Y. A novel recovery system for cultured cells using plasma-treated polystyrene dishes grafted with poly(N-isopropylacrylamide). J Biomed Mater Res 1993, 27:1243-1251.
38. Yang J., Yamato M., Kohno C., Nishimoto A., Sekine H., Fukai F., et al. Cell sheet engineering: recreating tissues without biodegradable scaffolds. Biomaterials 2005, 26:6415-6422.
39. Brun-Graeppi A.K., Richard C., Bessodes M., Scherman D., Merten O.-W. Thermoresponsive surfaces for cell culture and enzyme-free cell detachment. Prog Polym Sci 2010, 35:1311-1324.
40. Itabashi Y., Miyoshi S., Kawaguchi H., Yuasa S., Tanimoto K., Furuta A., et al. A new method for manufacturing cardiac cell sheets using fibrin-coated dishes and its electrophysiological studies by optical mapping. Artif Organs 2005, 29:95-103.
41. Ko I.K., Kato K., Iwata H. A thin carboxymethyl cellulose culture substrate for the cellulase-induced harvesting of an endothelial cell sheet. J Biomater Sci Polym 2005, 16:1277-1291.
42. Sakai S., Ogushi Y., Kawakami K. Enzymatically crosslinked carboxymethylcellulose-tyramine conjugate hydrogel: cellular adhesiveness and feasibility for cell sheet technology. Acta Biomater 2009, 5:554-559.
43. Ito A., Ino K., Kobayashi T., Honda H. The effect of RGD peptide-conjugated magnetite cationic liposomes on cell growth and cell sheet harvesting. Biomaterials 2005, 26:6185-6193.
44. Shimizu T., Yamato M., Kikuchi A., Okano T. Cell sheet engineering for myocardial tissue reconstruction. Biomaterials 2003, 24:2309-2316.
45. Akiyama H., Ito A., Kawabe Y., Kamihira M. Genetically engineered angiogenic cell sheets using magnetic force-based gene delivery and tissue fabrication techniques. Biomaterials 2010, 31:1251-1259.
46. Inaba R., Khademhosseini A., Suzuki H., Fukuda J. Electrochemical desorption of self-assembled monolayers for engineering cellular tissues. Biomaterials 2009, 30:3573-3579.
47. Seto Y., Inaba R., Okuyama T., Sassa F., Suzuki H., Fukuda J. Engineering of capillary-like structures in tissue constructs by electrochemical detachment of cells. Biomaterials 2010, 31:2209-2215.
48. Guillaume-Gentil O., Gabi M., Zenobi-Wong M., Voros J. Electrochemically switchable platform for the micro-patterning and release of heterotypic cell sheets. Biomed Microdevices 2011, 13:221-230.
49. Picart C. Polyelectrolyte multilayer films: from physico-chemical properties to the control of cellular processes. Curr Med Chem 2008, 15:685-697.
50. Crouzier T., Boudou T., Picart C. Polysaccharide-based polyelectrolyte multilayers. Curr Opin Colloid 2010, 15:417-426.
51. Brunot C., Grosgogeat B., Picart C., Lagneau C., Jaffrezic-Renault N., Ponsonnet L. Response of fibroblast activity and polyelectrolyte multilayer films coating titanium. Dent Mater 2008, 24:1025-1035.
52. Ren K., Fourel L., Rouviere C.G., Albiges-Rizo C., Picart C. Manipulation of the adhesive behaviour of skeletal muscle cells on soft and stiff polyelectrolyte multilayers. Acta Biomater 2010, 6:4238-4248.
53. Richert L., Arntz Y., Schaaf P., Voegel J.C., Picart C. pH dependent growth of poly(L-lysine)/poly(L-glutamic) acid multilayer films and their cell adhesion properties. Surf Sci 2004, 570:13-29.
54. Semenov O.V., Malek A., Bittermann A.G., Voros J., Zisch A.H. Engineered polyelectrolyte multilayer substrates for adhesion, proliferation, and differentiation of human mesenchymal stem cells. Tissue Eng Part A 2009, 15:2977-2990.
55. Richert L., Boulmedais F., Lavalle P., Mutterer J., Ferreux E., Decher G., et al. Improvement of stability and cell adhesion properties of polyelectrolyte multilayer films by chemical cross-linking. Biomacromolecules 2004, 5:284-294.
56. Boudou T., Crouzier T., Nicolas C., Ren K., Picart C. Polyelectrolyte multilayer nanofilms used as thin materials for cell mechano-sensitivity studies. Macromol Biosci 2011, 11:77-89.
57. Boudou T., Crouzier T., Auzely-Velty R., Glinel K., Picart C. Internal composition versus the mechanical properties of polyelectrolyte multilayer films: the influence of chemical cross-linking. Langmuir 2009, 25:13809-13819.
58. Moussallem M.D., Olenych S.G., Scott S.L., Keller T.C., Schlenoff J.B. Smooth muscle cell phenotype modulation and contraction on native and cross-linked polyelectrolyte multilayers. Biomacromolecules 2009, 10:3062-3068.
59. Ngankam A.P., Mao G., Van Tassel P.R. Fibronectin adsorption onto polyelectrolyte multilayer films. Langmuir 2004, 20:3362-3370.
60. Wittmer C.R., Phelps J.A., Saltzman W.M., Van Tassel P.R. Fibronectin terminated multilayer films: protein adsorption and cell attachment studies. Biomaterials 2007, 28:851-860.
61. Ball V., Hubsch E., Schweiss R., Voegel J.C., Schaaf P., Knoll W. Interactions between multivalent ions and exponentially growing multilayers: dissolution and exchange processes. Langmuir 2005, 21:8526-8531.
62. Boulmedais F., Ball V., Schwinte P., Frisch B., Schaaf P., Voegel J.C. Buildup of exponentially growing multilayer polypeptide films with internal secondary structure. Langmuir 2003, 19:440-445.
63. Picart C., Lavalle P., Hubert P., Cuisinier F.J.G., Decher G., Schaaf P., et al. Buildup mechanism for poly(L-lysine)/hyaluronic acid films onto a solid surface. Langmuir 2001, 17:7414-7424.
64. Weder G., Guillaume-Gentil O., Matthey N., Montagne F., Heinzelmann H., Voros J., et al. The quantification of single cell adhesion on functionalized surfaces for cell sheet engineering. Biomaterials 2010, 31:6436-6443.
65. Picart C., Mutterer J., Richert L., Luo Y., Prestwich G.D., Schaaf P., et al. Molecular basis for the explanation of the exponential growth of polyelectrolyte multilayers. Proc Natl Acad Sci USA 2002, 99:12531-12535.
66. Guillaume-Gentil O., Zahn R., Lindhoud S., Graf N., Voros J., Zambelli T. From nanodroplets to continuous films: how the morphology of polyelectrolyte multilayers depends on the dielectric permittivity and the surface charge of the supporting substrate. Soft Matter 2011, 7:3861-3871.
67. Mjahed H., Voegel J.C., Senger B., Chassepot A., Rameau A., Ball V., et al. Hole formation induced by ionic strength increase in exponentially growing multilayer films. Soft Matter 2009, 5:2269-2276.
68. Mertz D., Vogt C., Hemmerle J., Mutterer J., Ball V., Voegel J.C., et al. Mechanotransductive surfaces for reversible biocatalysis activation. Nat Mater 2009, 8:731-735.
69. Szarpak A., Cui D., Dubreuil F., De Geest B.G., De Cock L.J., Picart C., et al. Designing hyaluronic acid-based layer-by-layer capsules as a carrier for intracellular drug delivery. Biomacromolecules 2010, 11:713-720.
70. Wang B., Anzai J. Redox reactions of ferricyanide ions in layer-by-layer deposited polysaccharide films: a significant effect of the type of polycation in the films. Langmuir 2007, 23:7378-7384.
71. Nagai N., Yunoki S., Satoh Y., Tajima K., Munekata M. A method of cell-sheet preparation using collagenase digestion of salmon atelocollagen fibrillar gel. J Biosci Bioeng 2004, 98:493-496.
72. Hubsch E., Fleith G., Fatisson J., Labbe P., Voegel J.C., Schaaf P., et al. Multivalent ion/polyelectrolyte exchange processes in exponentially growing multilayers. Langmuir 2005, 21:3664-3669.
73. Zahn R., Boulmedais F., Voros J., Schaaf P., Zambelli T. Ion and solvent exchange processes in PGA/PAH polyelectrolyte multilayers containing ferrocyanide. J Phys Chem B 2010, 114:3759-3768.
74. Wang B., Noguchi T., Anzai J. Layer-by-layer thin film-coated electrodes for electrocatalytic determination of ascorbic acid. Talanta 2007, 72:415-418.
75. Fischer D., Li Y., Ahlemeyer B., Krieglstein J., Kissel T. In vitro cytotoxicity testing of polycations: influence of polymer structure on cell viability and hemolysis. Biomaterials 2003, 24:1121-1131.
76. Chanana M., Gliozzi A., Diaspro A., Chodnevskaja I., Huewel S., Moskalenko V., et al. Interaction of polyelectrolytes and their composites with living cells. Nano Lett 2005, 5:2605-2612.